Published in the United States of America
— 2019 e VOLUME 13 « NUMBER 2
AMPHIBIAN & REPTILE
CONSERVATION
IN wes to William R. Branch
(1946-2018)
amphibian-reptile-conservation.org
ISSN: 1083-446X eISSN: 1525-9153
Cover photo legend, in Bill’s own words:
This remains one of my favourite shots, although it is an old slide and this is the best digital scan | have of it (but of
woefully low res). It was taken about 25+ years ago, and | was driving to work when | saw these flowers in bloom beside
Port Elizabeth airport. | had an image of a cobra rearing in front of them, the Port Elizabeth Snake Park had just got
a beautiful Cape Cobra in from the Northern Cape, and so | asked Rob Hall to come and help manipulate the snake.
| didn't have a long lens and so had to lie on my belly with a 55mm Nikkon with 1.4 convertor. | used in-fill flash, held
by Rob about 1m away and to soften the deep shadow under the snake's belly. | kept shuffling forward to get a more
dramatic pose and had taken several shots when the snake disappeared from the viewfinder. Rob was standing to the
side holding the flash and also a snake stick to ward off the cobra. When the snake disappeared | instinctively rolled
back, heard Rob shout "Shit, that was fast!", and the snake bit the camera body about 6cm from my shutter finger. A
bead of venom glistened on the camera body. Looking through the lens | had lost all sense of distance and simply got
too close to the snake. It remains the closest I've come to a snakebite. Technically the picture works because the snake
is alert but its mouth is shut and it is not looking straight at the camera. It therefore doesn't appear too threatening,
allowing viewers to admire what remains my favourite snake. Bill Branch
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: i-—xxix (e186).
Compilation of personal tributes to William Roy Branch
(1946-2018): a loving husband and father, a good friend,
and a mentor
1*Werner Conradie, *7Michael L. Grieneisen, and *Craig L. Hassapakis (Editors)
'Port Elizabeth Museum (Bayworld), P.O. Box 13147, Humewood 6013, SOUTH AFRICA *School of Natural Resource Management, George
Campus, Nelson Mandela University, George 6530, SOUTH AFRICA *Department of Land, Air and Water Resources, University of California,
Davis, California 95616, USA *Amphibian & Reptile Conservation (amphibian-reptile-conservation.org) and Amphibian Conservation Research
Center and Laboratory (ACRCL), 12180 South 300 East, Draper, Utah 84020-1433, USA
Abstract.—Personal contributions to William “Bill” Roy Branch by famly members and colleagues: Colin
Tilbury, Alan Channing, Dot Hall (Pitman, Basson), Rick Shine, James B. Murphy, Luke Verburgt, Julian Bayliss,
Michael F. Bates, Pedro Vaz Pinto, Kirsty Kyle, Krystal Tolley, Mzi Mahola, Brian J. Huntley, Roger Bills, Johan
Marais, Mark-Oliver Rodel, Paul H. Skelton, Aaron M. Bauer, Stephen Spawls, Andrew Turner, Ernst H.W. Baard,
Amber Jackson, Margaretha Hofmeyr, Jens Reissig, Harold Braack, Atherton de Villiers, Marius Burger, Mike
Raath, Werner Conradie, and Martin J. Whiting.
Keywords. Influence, contributions, farewell, African herpetology, history, researcher
Citation: Conradie W, Grieneisen ML, Hassapakis CL (Editors). 2019. Compilation of personal tributes to William Roy Branch (1946-2018): a loving
husband and father, a good friend, and a mentor. Amphibian & Reptile Conservation 13(2) [Special Section]: i—xxix (e186).
Copyright: © 2019 Conradie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 5 August 2019; Accepted: 5 August 2019; Published: 10 September 2019
On 14 October 2018, William Roy Branch, or simply
Bill as he was known to most, passed away after a short
struggle with motor neuron disease. He was not only
one of South Africa’s most well-known and respected
herpetologists, but also a dedicated husband, a father, a
good friend, and a mentor to so many of us. We have
taken this opportunity to collate personal tributes from
family, friends, and colleagues, to showcase the influence
Bill had on our lives and careers.
Tributes from family members
Donve Branch (Bill’s wife)
Bill was an amazing man with a huge passion for life.
When we married I introduced Bill to the world of
pots and potters, and he introduced me to the world of
reptiles and herpetologists. Very different worlds, but
they became one we both loved. Over the years I was
privileged to meet and host many of you. If I sometimes
looked stunned when you arrived at our door, please
forgive me. Bill very often failed to tell me we would
be having a guest. Together we started to collect art,
succulents, and books. None of which we could afford,
Correspondence. * werner@bayworld.co.za
Amphib. Reptile Conserv.
but we couldn’t resist.
Bill was a family man who loved and was so proud of
his three sons. When we married his generous heart took
on my children and grandchildren with the same warmth.
Science was his passion which he loved to share. Bill in
lecture mode could not be halted. His sense of humour
was legendry. A kind, gentle man but also a humble
man. He never boasted of his achievements. In his later
years, these qualities made him so popular with National
Geographic travellers.
A man of huge intellect with a broad knowledge of
all things. A kind, generous, and wonderful man. Truly a
real mensch. I was so proud to be his wife. He is greatly
missed.
James Vlok (Bill’s stepson)
Bill Branch was a man of passion for his craft and
natural science. He was an adventurer and an explorer;
a man who inspired motivation and discovery of the
world around us. He could keep you interested with a
keen knowledge and a sense of humour that would have
you laughing and learning. He will be sorely missed by
family and colleagues alike.
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
Christian Vlok (Donveé’s grandson)
Gumps told me so many interesting stories about his
trips. He gave me my first Masai machete and a lizard. I
knew I could ask him anything and he would know the
answer. I will miss my Grandpa Gumps so much.
Analeah Vlok (Donve’s granddaughter)
I loved Gumps because he taught me so many things.
He taught me which plants I can or can't eat, and about
snakes and frogs, which I love. I miss him and every time
I go into his room I think of him.
Jenny Vlok (stepdaughter-in-law)
Bill, to look at all things herpetological on a daily basis
and know that I can't ask you any more questions about
it, fills my heart with such sadness. You were so patient
in your explanations, always interesting and funny. With
your mismatched socks and wild hair, your fancy salads
and poor man's capers, hilarious Easter egg hunts with
a difference, cheeky Halloween surprises and Christmas
gifting, not only were you an Amazing scientist but also
an inspiration, and a motivator, allowing my children
to be knowledge bearers and researchers in their own
environment. We love you Dear Bill, and will miss you
always.
Nicole Kingston (Bill’s stepdaughter)
Bill was a rock, a voice of reason, and a safe place and
so loved. I am so truly privileged to have known him,
and am a better person for it. His kindness, empathy, and
wicked sense of humour will not be forgotten.
Oliver Kingston (Donve’s grandson)
Grandpa made me laugh lots and 1f you wanted to know
anything he was the person to ask.
Will Kingston (Donve’s grandson)
He was kind and knew a lot about snakes.
Tributes from friends and colleagues
Colin Tilbury
KwaZulu-Natal, South Africa
It was early in 1980. After a year as a junior medical officer
at Ngwelezana Hospital in KZN [KwaZulu-Natal], I had
collected a series of cases of snakebites from Atractaspis
bibronii and the Mozambique Spitting Cobra. With the
data in hand I had approached Alan Channing, the then-
chairman of the Herpetological Association of Africa,
for comments. Being more of the toad persuasion,
Alan suggested that I contact his colleague Bill Branch,
the incumbent curator of herpetology at the PE [Port
Elizabeth] Museum, who had shown more than just a
passing interest in snakes and snakebite, and might be in
Amphib. Reptile Conserv.
a better position to help me.
I wrote to Bill and offered to assist with any affairs of
the herpetological kind from Zululand. Bill wrote back
immediately, expressing a keen interest in the snakebite
data and also wondering if I might be able to collect some
of the local Pelusios for karyotyping. We met for the
first time a few months later. Bill was visiting Durban,
and Sarah and I arranged to meet him at the British
Middle East Indian Sporting and Diners’ Club near the
Greyville race course, to sample the local curries. A truly
memorable evening (I still have intermittent diarrhoea). I
think that I may also have introduced Bill to the pleasures
of a good red wine—or was it vice versa?
And so began a friendship which lasted nearly 40
years.
Driven with a boundless energy and an amazing
zest for life, sharp wit, wry humour, and capacity for
sharing, Bill attracted people to him. Whether by active
involvement or by association, he had a lasting impact
on all those who encountered him. Bill adored the simple
things in life, and lived his life simply. He loved the
camping and field trips that were an integral part of his
work and which provided him with so much satisfaction.
An avid angler since childhood, he had pulled many a
carp from the rivers and dams of the Eastern Cape. Bill’s
laboratory and office in the Port Elizabeth Museum was
always a wondrous place to visit. Beyond the entrance
door which was plastered with a selection of humorous
“Bill” references, a mixture of chaos and creativity,
preserved snakes and lizards in piles, the air reeking
with alcohol, and Bill smiling happily. Bill and Donveé’s
lovely home in Port Elizabeth was in many ways an
extension of his beloved office at the museum. Of the
many enduring mental images that capture Bill’s essence
for me, are none more so than those of Bill at work in
his man-cave at home. More like a ‘control room,’ his
desk surmounted with massive computer screens and
surrounded on all sides—floor to ceiling—with books,
paintings, and photographs (including his all-time
favourite of the yellow Cape Cobra that had nearly bitten
him). Shelves were packed with w.1.p. files and books
with titles covering an eclectic array of topics from
tadpoles to volcanoes, fossils, sunbirds, euphorbias,
mesembs, and every conceivable reptile and amphibian
genre.
At home, but outside his study, every nook and cranny
was adorned with paintings and Donve’s beautiful
pottery. Each windowsill in the house was crammed with
weirdly-shaped, rare, and spiky plants. Their garden was
an indigenous plant paradise with a few thorny exotics,
a haven for birds and local wildlife where the largest
Palystes rain spiders in the world were free to roam—
although strangely I only ever saw them on the walls of
the guest bedroom. Theirs was clearly a home they loved
to live in and was always open to the many guests who
might pop in and stay over.
September 2019 | Volume 13 | Number 2 | e186
Conradie et al.
One could not know Bill and be unimpressed with
his amazing intellect. Bill read—-no—he devoured books
by the ton. I have never met anyone who had such a
command and broad understanding of natural history. He
could have been anything from botanist, ornithologist,
entomologist, mammologist, geologist, physicist—you
name it. The reality in fact, is that he was all of these
things and many more; such was the breadth and depth
of his knowledge. His intimate understanding of the
intricacies of natural history, the environment, and the
interconnected webs of life, filling in the dots on life’s
canvas one by one—or in Bill’s case, by the dozens at
a time.
In spite of his huge talents, he kept his feet firmly on
the ground and freely shared his knowledge and wisdom
with anyone who asked for advice or input. He was an
inspirational force to anyone and everyone who had the
privilege to know or work with him; a truly benevolent
gentle giant and an incredibly productive scientist. The
herpetological community around him was so privileged
to have him as a guide and mentor. In the decade following
his retirement from the museum, he worked as a specialist
guide for over 50 National Geographic touring parties.
These afforded him opportunities to continue to pursue
herps in many iconic African locations.
As a friend, Bill was caring, insightful, non-
judgmental, and always with a wonderful sense of
humour just bubbling beneath the surface. As a storyteller
he had few peers: in his clipped British accent with the
hint of a lisp mumble and a wry smile, he would gleefully
extol the excruciating agony of the many unfortunates
who became the subjects of his tales. Of course, these
often involved his hapless colleagues on the many field
trips that he made. Quick, dry, wicked, invariably veiled
in intrigue, he would construct the twists and turns of
his story to extract every molecule of humour. His punch
lines always immaculate.
Over the years, I spent a great deal of time outside the
borders of South Africa, but Bill always found time to
write and give updates on his projects and movements.
After the birth of our first child in London in July
1989, Sarah and I sent out a short notice of his birth
to a few friends and relatives, making reference to ‘the
discovery of a new species of the TILBURY genus found
lurking in the St Helier 's Labour Ward at precisely 03h45
hours on 25 July 1989. It is wriggly, pink all over, devoid
of scales and tail, and makes characteristic feeding cries
every 4 hours. It weighed 3.63 kg on discovery, and has
the features characteristic of the male sex. It has been
named Douglas Matthew.”
I left London a week after the event and headed back
to my job in Saudi Arabia. Shortly after my return to
Khamis Mushayt, I received a letter from Bill:
“Dear Colin,
Congratulations on the arrival of Douglas Matthew.
You must be looking forward to Sarah and DMT
Amphib. Reptile Conserv.
arriving at the end of the month, although I suppose
that throwing all the Cerastes out to make way for the
cot must be a bind. He will slow your globe-trotting
down a bit, but it will only be about 12 years before
he is useful in the field! Robbie and Matthew do all
the hard work in the field now, so they do have their
advantages.
[feel | must take exception to the new name however.
Looking through the London telephone directory I
came across three other references to Tilbury Douglas
Matthew (usually from the poorer eastern suburbs
besides the Thames). All had priority, some dating from
the early 1930's. Your new name is thus pre-occupied,
and according to strict nomenclatural rules (Int. Rules
Zool. Nomenclature, rev. ed. London 1986; page 25,
paragraph 3), becomes a strict junior homonym and
is invalid. As well as afflicting the young lad with a
used name, it is also incorrectly formed according
to the rules governing construction of names. Being
the first scientist (of truly international standing) to
have spotted this error, I claim my right to propose a
replacement name. I have chosen:
Tilburyanus inhirsutus arabicum Branch 1989
You will note that the Generic name is now correctly
Latinized and the ending is more appropriate
(being his most obvious feature for the moment!).
The specific epithet also refers to the sub-adult
plumage, while the sub-specific name is a traditional,
uninspiring geographical allocation. Knowing that he
is now correctly named, you may re-apply for birth
certificates, passports and driving licences etc.”
For a man who played with snakes, Bill had a simple
philosophy. Respect them and you won’t get bitten,
and as far as I know, apart from a single dry bite from
a Thelotornis, he never did. I remember the day that I
brought a small shiny black snake all the way from
the DRC [Democratic Republic of the Congo] to Bill’s
home, and proudly handed him the blue cotton bag that
contained the snake which I had carefully nurtured for
the previous month or so. Bill gleefully but carefully
opened the bag and peered inside. Then to my horror, he
inserted his hand into the bag to retrieve the snake.
I said ‘Whoa! Hang on there a minute; I just want to
get out my notebook and camera to record the first bite
from this unknown species of Atractaspis.’ Bill pulled
out his hand, the snake dangling limply between his
fingers. Rigor mortis had already worn off.
“You've killed it” I said.
IN Oe ete nit excuses Do you think it is a Norwegian
Blue?” (A joke that can only be appreciated by followers
of Monty Python).
But it was not only herps that Bill would talk about.
As much as he was a scientist, he was also a profoundly
loved family man who would talk with pride as much
about his loved ones as he would about his work. Give
him half a chance and he would talk for hours about his
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
sons Robbie, Matthew, and Tom and his new family—
Nicole, Anthony, and James.
It was in 2012 that Bill first realised that he was
only human after all, when he contracted malaria in
Mozambique. That nearly finished him off. He eventually
bounced back to his old self, but he was unable to dodge
the bullet of MND [motor neuron disease]. When Bill
contacted me in February 2018 to say that he had been
diagnosed, it felt as if a tree had fallen on me. I had the
good fortune to be able to spend several days with Bill
over the last months of his life; and to be able to share
memories of the good times, laugh together, discuss the
iniquities of life, and to acknowledge the simple fact that
we are all just fulfilling our biological destiny—albeit in
different ways.
One cannot write about Bill without acknowledging
the major part in his life that Donvé played, as his partner
and soul mate, and in turn appreciate the huge hole that
has been left behind by his passing in Donve’s life. In
one conversation we had, we both agreed that it was one
of the greatest privileges of life to be able to love and be
loved back unconditionally. I don’t think that anyone can
overestimate the enormity of this gift. She made him so
happy and in the end, so sad that his Dove would have
to endure the last days of his life with him in the state he
was in.
Bill asked me to sign as witness to his living will to
not be placed on any mechanical machine that would
prolong his life. As his MND advanced, even in the late
stages, in spite of his body being totally paralysed, his
mind was as lively as ever; as he fought day by day to
extract, utilise, and enjoy to the last moment every second
that was left to him. He was immensely saddened and so
disappointed that he had run out of time to complete all
the many projects that he was part of or had initiated.
His illness had quite literally pulled the rug out from
beneath his feet. I know that Bill handed over many
of these to colleagues to finish—we should make him
proud. Even as he inexorably neared the end, he was so
brave in facing his fate. He could still make jokes about
this. He once compared himself as a likeness of the blue-
headed agamid that was named after him (Acanthocercus
Fig. 1. Cover image of Hyperolius raymondi used for Frogs and
other Amphibians of Africa (Photo: Bill Branch).
Amphib. Reptile Conserv.
branchi). Finally in the afternoon of 14 October, dulled by
the ever-increasing CO, levels, he finally and peacefully
breathed his last. The end to a magnificent life. His was
an act we could all learn something from.
More than anyone, Bill understood and appreciated the
fact that no one gets to live forever, but that everyone is
hopefully gifted with the opportunity to leave a footprint
embedded in the rocks of humanity—a footprint that will
endure with a permanent relevance to those who follow
one’s trail. Bill had big feet for such a small frame, and no
doubt we will be following his prints for many a year. I can
only say that I was privileged to know Bill, and even more
so, to think that he might have considered me to be a friend.
The memories of Bill will be enduring and he will
always be celebrated as one of the world’s leading
herpetologists of our time. He will be sorely missed and
long remembered.
Alan Channing
University of the Western Cape/North-West University,
South Africa
I met Bill at a herp meeting while he was working at
the Atomic Energy Board in the 1970s. He was hugely
enthusiastic and well-read. Later, I was happy to support
his application for the post of Herpetologist at the Port
Elizabeth Museum, when asked by the Director. We
undertook many field trips together, and for a while we
formed a collaboration for funding from the forerunner
of the National Research Foundation.
Although Bill and I worked on different groups, there
was always a lot of friendly banter between us. His sense
of humour was displayed on one field trip to northern
Namibia, when he offered to cook the potatoes, while I
prepared the meat. When it came time to eat, the potatoes
were still crunchy. Bill's response was to explain that that
was how they were cooked in Cornwall, and that it was a
classical culinary procedure!
I will miss Bill's insights and our regular email
exchanges. He provided a number of excellent photos
for the upcoming book Frogs and other Amphibians of
Africa, and was always willing to help, or offer a beer
and a meal, when I was in Port Elizabeth.
as - i =
Fig. 2. Bill p otographing a lizard in southern Angola, 18
January 2009 (Photo: Alan Channing).
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Conradie et al.
Dot Hall (Pitman, Basson)
Port Elizabeth Museum (Bayworld), South Africa
A flood of memories flow through my mind when I
reminisce on the very small part of Bill’s life I shared.
One in particular always makes me smile. When Bill
joined the Museum in 1978, he was a complete unknown.
We were observing his introduction to the staff with
interest: A quiet, rather serious little man? From his first
day he was a regular library user. He was passionate
about books. Each visit he made to it was a learning
experience for me. He freely shared his knowledge and
always stretched my way of thinking.
On one memorable morning, shortly after he had
joined the staff, all was quiet in the library when a strange
scuffing noise caught my attention. No-one was in the
library, so I put this observation down to my imagination
and continued working. The same noise recurred several
times till I eventually decided to investigate. There was
a solid counter that separated the librarian from those
using the library. I peered over this counter to find Bill
on all fours, crawling behind a large leguaan [varanid]
holding its tail and trying to direct it around the corner
to my desk. I guess it was being a little uncooperative
and his full attention was required for him to achieve his
goal—“Frighten this librarian out of her mind!!!” After
observing the scene for a short while I decided to launch
a surprise “attack” from the back and gave him a pinch
on his rear end. His reaction was marvellous. The leguaan
was let loose and his fright was complete.
Fig. 3. Bill Xerox-ing a puffadder to make counting of scales
easier, to the disgrace of the librarian (Photo: Dot Pitman).
Amphib. Reptile Conserv.
We both enjoyed sharing this amusing moment.
How many million more smiles has he given to the vast
number of people with whom he associated?
Rick Shine
Macquarie University, Australia
I first met Bill Branch on the morning of Tuesday the
5th of September 1989, at the British Museum of Natural
History (now the Natural History Museum London).
Like me, he had travelled to the UK to attend the First
World Congress of Herpetology, and like me, he took
advantage of the opportunity to visit the British Museum
of Natural History. Bill was looking for type specimens
of African herps, and I was attempting to track down
the reptile specimens that Charles Darwin collected in
Australia during the voyage of the Beagle. As we sat
and talked over lunch, I was astonished at Bill’s breadth
of knowledge about the African herpetofauna, and his
intimate familiarity with the scientific literature on those
animals. But I had no idea that we would end up as
collaborators on a major project.
Five years later, I took my first (and only!) sabbatical
from the University of Sydney. My wife Terri and I
had always wanted to see the famous game reserves of
southern Africa, and our oldest son was about to turn
12—after which time he would have to pay a full fare
on the airlines rather than half-price! So I contacted
Bill about the possibility of dissecting preserved snakes
in African museum collections for ecological data
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September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
POFADDER é
(gut contents, gonads, etc.) as I had done for snakes in
Australian museums over the previous years. Bill was
enthusiastic, but thought that the best collection might be
in Namibia, where over 1,500 snakes that had drowned
in an open canal (the Eastern Water Carrier) had been
preserved by the local wildlife authorities. And with the
first South African elections looming, and political unrest
likely as power shifted from ‘Afrikaaners’ to native
Africans, Namibia looked like a quieter, safer option than
South Africa for a family with 10-year-old and 2-year-
old children.
We flew to Namibia while Bill drove the museum’s
Kombi-van from Port Elizabeth to Windhoek to meet us.
And being Bill, he had a much better idea than staying in
Windhoek to dissect the snakes—instead, we piled them
into the van and took off for Gobabeb, where we could
enjoy the spectacular dunes in between long hours of
peering inside dead snakes. The Aussie team (me, Peter
Harlow, and Jonno Webb) peered inside the innards of
dead snakes and called out numbers, while Terri wrote
them all down into data-sheets. Bill carefully examined
every half-digested frog and reptile that came out of a
snake stomach, almost always managing to ID it, even if
he only had a few toes to work with. It was a happy and
effective team.
After we finished the Namibian snakes, my family
flew off to the USA while the rest of us drove down to
Pretoria to look at MORE snakes at the national museum
in Pretoria. It was a classic herp “road trip,” with frequent
detours to look for specific taxa (usually, so that Bill
could get a photograph for his field guide). We made an
obligatory stop at Poffadder (= “Puff Adder’) one of the
few towns named after a snake, near the border between
South Africa and Namibia. A photograph I took on the
town’s outskirts captures the relaxed joy of herpetological
zealots indulging their passions (Fig. 5). We worked
long hours in Pretoria, obtaining a mountain of data that
eventually translated into 15 papers on the natural history
of several major lineages of African snakes. We also
sampled the local beer and watched World Cup soccer
games at bars downtown—horrifying some of the locals
who were convinced that we would be mugged as we
walked the streets at night.
Throughout this first African adventure, Bill was
fantastic. Extraordinarily knowledgeable, with a vast
network of contacts, he made the project possible. We
talked long and often about everything from fishing
to the mysteries of bureaucracies and families—and
especially, about snakes. Hopping off a plane and looking
inside preserved specimens can generate a lot of data—
but it was Bill’s long experience that enabled us to put
that information into context. For many of the species
about which we wrote papers, I had never even seen a
live specimen—but Bill had, and his firsthand knowledge
helped him to laugh off my ill-informed speculations,
and keep our interpretations true to the reality of snake
ecology in southern Africa. Bill was a terrific collaborator
Amphib. Reptile Conserv.
vi
MY
a
Fig. 5. Jonno Webb, Bill Branch, and Peter Harlow posing at
the outskirts of the town of Poffadder in northern South Africa,
reveling in the idea that somebody actually named a town after
a snake (Photo: Rick Shine).
Pet i
and a wonderful friend. I feel privileged to have been
able to work with him.
James B. Murphy
Division of Amphibians & Reptiles, National Museum
of Natural History, Washington DC, USA
When we first met at a herpetological conference in the
US many years ago, Bill and I noticed that our love of
amphibians and reptiles, overall biological interests, and
personal histories were strikingly parallel. One major
difference was that Bill had completed a Ph.D. inchemistry
and I barely passed my chemistry courses. Fortunately,
he changed trajectories and excelled in herpetology. As
we shared our stories over some beers until the break
of dawn, Bill and I quickly bonded. I invited him to
come to Dallas, Texas, where I was herp curator at the
Dallas Zoo with a spacious guest room available in my
home. As we toured the Zoo’s herp collection, Bill was
delighted when he saw the large breeding group of New
Caledonian Geckos (Rhacodactylus leachianus, Fig. 6).
There was a particularly large and impressive male that
was surplus, so I gave it to Bill—his stunned reaction
and gratitude were wonderful to watch as he carefully
packed the saurian to hand-carry it back to Port Elizabeth
[ED note: This gecko is still alive in the Port Elizabeth
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Conradie et al.
Museum as of July 2019].
After the First World Congress of Herpetology in
Canterbury, UK, he invited me to stay at his parents’
home nearby until we later went to Bonn, Germany,
for the first Varanid Symposium held at the Museum
Alexander Koenig (Fig. 7). In my view, Bill was a
pretty stocky fellow, but his mother was concerned that
he was not paying enough attention to proper nutrition,
so she followed him for several days with handfuls of
vegetables, insisting all the while that he was becoming
a mere slip of a man. The scenario reminded me of a
Monty Python skit.
At the varanid meeting, Bill presented a wonderful
lecture on the White-throated Monitor (Varanus
albigularis)—“The Regenia_ registers of Brown
(1869-1909). Memoranda on a species of Monitor or
Varan.” Branch covered all aspects of Alfred ‘Gogga’
Brown’s extensive observations—sex ratio, size, body
proportions, hemipenial morphology, visceral fat bodies,
coloration, diet, cause of death, longevity, reproduction,
gestation period, egg laying, oviposition, eggs, clutch
size, hatchling size, incubation period, growth, behavior,
mating behavior, shedding, thermoregulation, predation,
parasites, exploitation, and seasonal activity and retreats.
The amount of information that Gogga had collected on
his captive lizards and in wild counterparts in the late
19th century is truly astounding.
Over time, Bill sent anumber of African and Namibian
reptiles for the Dallas Zoo collection, including Angulate
Tortoise (Chersina angulata), Parrot-beaked Tortoise
(Homopus_ areolatus), Tent Tortoise (Psammobates
tentorius), Mountain Adder (Bitis atropos), Dwarf Adder
(Bitis rubida), Many-horned Adder (Bitis cornuta), Cape
Dwarf Chameleon (Bradypodion pumilum), Lesser Flat
Lizard (Platysaurus guttatus), and Drakensberg Crag
Lizard (Pseudocordylus subviridis).
In the ensuing years, we spent much time together
at meetings and he shared his concern about shrinking
funding for the Port Elizabeth Snake Park and Museum.
Frederick William FitzSimons (born 1875) was the first
Director of the Museum in 1906, and he developed the
Fig. 6. Male New Caledonian Geckos (Rhacodactylus
leachianus) still alive in Port Elizabeth Snake Park (Photo:
Werner Conradie).
Amphib. Reptile Conserv.
vil
Fig. Z Varanid Symposium participants at Museum Alexander
Koenig in 1991. Bill Branch is the seventh person from the left,
in the front row.
Snake Park. His son, Vivian, assisted him and both of
them published in herpetology. His younger brother,
Desmond C. FitzSimons, started the Durban Snake Park.
F. W. FitzSimons also wrote books on the natural history
of South African mammals, including primates.
Bill was a consummate biologist whose contributions
to our knowledge of African amphibians and reptiles over
several decades set the high standard for herpetological
work. His nominal retirement as curator of herpetology
at the Port Elizabeth Museum occurred after many years
of service. As far as I know, he did not free-handle
venomous snakes nor put them on his head. Every time
we met, I could be confident that he would cover subjects
virtually unknown to me. He will be missed.
Luke Verburgt
Enviro-Insight & University of Pretoria, South Africa
Bill replied to my email almost instantly and in great
detail! I'd been very hesitant to contact my herpetological
idol about a reptile identification query, because I guess
I was afraid to disturb such an important person with
possibly silly and trivial queries from me, a nobody.
Yet to my delight, Bill took the time to carefully answer
my questions, providing great detail and assistance.
No admonishment for not having read the appropriate
books/papers, and no arrogant stance regarding my lack
of herping credentials! I was thrilled, and it opened up
communication between us to such an extent that soon
we were communicating about African herpetofauna via
email quite regularly, with Bill always helpful and kind
in dispensing his amazing wealth of knowledge. Like a
mentor really.
I eventually met Bill in person months later in
Namibia, along with Johan Marais and Aaron Bauer,
while they were on a collecting field trip. It was such
an honour to be sitting around the same table as these
herping heroes, and I was rather star-struck. After some
fieldwork with the team, I picked up on the fact that the
species of Rhoptropus that we were collecting was not
the one I had expected to be there according to Bill’s
field guide, which was really my main source of herp
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
knowledge, as it has also been for so many others.
I eventually plucked up the courage and cautiously
approached Bill one afternoon, to ask about this
Rhoptropus situation. He laughed heartily and said,
“Oh, that map is complete rubbish!" I couldn't believe it.
The author of the book that I cherished above all others
just told me that some of it wasn't the complete truth!
And right there I learned two massive lessons from Bill
about African herpetology: imperfect data from under-
sampling abound, and not being afraid to question the
existing understanding.
Sadly, that was the one and only time I got to be in
the field with Bill, and it was far too brief. Thankfully
though, we collaborated a lot after that with several
resulting papers where I got to be a co-author with
Bill—a huge honour! However, the greatest honour
for me in this regard was having Bill as a co-author
guiding my very first reptile species description, an
interaction through which I learnt more than I could've
ever imagined. He took what was a pretty ordinary and
mundane manuscript and guided me on how to improve
it to an acceptable standard, the standard which he was
instrumental in setting for African herpetology.
After that I regularly reported to Bill, who was always
extremely interested in my findings because I was often
working in poorly sampled rural places across Africa.
In his now familiar mentor role, he would encourage
me to do as much useful sampling as possible, and
also to think harder about why a particular species was
observed in the habitat I found it in and, therefore, to
consider its ecology in greater detail and gain more
insight from my observations. In short, Bill made me
a better herpetologist and I am forever grateful for his
friendship and his mentoring.
Although I didn’t see Bill in person very often, it was
always a treat to hang out with him and his fantastic
sense of humour. But what I think I enjoyed the most
was to hang out with him and to see him having such
fun at the 2017 HAA conference at Bonamanzi, and
I was even lucky enough to win a “selfie” with him!
Unfortunately, I never actually received the “selfie’—
but fortunately, Shivan Parusnath managed to capture
the “selfie”’-taking moment perfectly, and it is my
favourite photo of Bill and myself (Fig. 8).
I received the news that Bill had passed away while
I was sampling in the Cabinda Province of Angola, an
area of great interest for Bill. While we all had known
for some time that it was an inevitability, the news of
his passing came as a massive shock to me because
only a few hours earlier, during his last night, Bill had
somehow managed to send me a lengthy Whatsapp
message, instructing me to collect as many DNA samples
of certain species as I could due to the importance of the
sampling locality I was in. And thinking about it now,
that's just how it was always going to be for Bill, the
ever-enthusiastic herpetologist and helpful mentor to
the very, very end. Rest easy Bill, I miss you so much
Amphib. Reptile Conserv.
viii
AANA
Fig. 8. Taking a “selfie” with Bill as part of the prize for
runner-up best photographer (Photo: Shivan Parusnath).
and hope that I am able to justify the effort you put into
sharing your time and knowledge with me.
Julian Bayliss
Ecologist and Explorer, Wales
I first met Bill when he came to undertake a
herpetological survey on Mount Mulanje in Malawi with
Johan Marais and Michael Cunningham in 2005, as part
of the ongoing ecological monitoring programme on
Mulanje that I was coordinating. However, it was really
when we met the second time, when Bill and Werner
Conradie joined me on Mount Mabu in 2009, that we
really got to know each other well. I had been working
the mountains of northern Mozambique for several
years prior to this event, and had managed to turn up
several new species of snakes and chameleons, although
my herp work was opportunistic (I discovered Atheris
mabuensis by stepping on it!) and I needed professional
assistance (Fig. 9). These discoveries attracted Bill, and
we arranged for a trip to Mt. Mabu forest to collect more
specimens, and also to see if we could collect specimens
of a Nadzikambia chameleon that was only known from
a couple of photographs taken on my previous visits.
We were successful in this endeavour, and I managed
to collect the first specimen of the Nadzikambia from
Mt. Mabu which Bill named after me as Nadzikambia
Fig. 9. Photograph of Atheris mabuensis taken by Bill—
probably the best photograph of a snake I have ever seen
(Photo: Bill Branch).
September 2019 | Volume 13 | Number 2 | e186
Conradie et al.
Fig. 10. The Mt. Mabu 2009 science team. Left to right:
Werner Conradie, Martin Hassan, Julian Bayliss, Bill Branch,
Hassam Patel, Colin Congdon, and Steve Collins (Photo:
Julian Bayliss).
baylissi. | was deeply honoured by this gesture.
The 2009 Mt. Mabu expedition proved to be a
very enjoyable expedition, packed full of laughter,
good company, and good food. I had also invited the
butterfly crowd from the African Butterfly Research
Institute (ABRI), a great bunch of eccentrics, and the
stories flowed around the camp fires at night. At the end
of the expedition, we all stood below a large tree on
the forest camp in Mt. Mabu with Bill at centre stage
(Fig. 10). This is one of my favourite photos of Bill,
and it captures a moment in time where nothing outside
that camp at that time really mattered. This was the
start of a very good friendship with Bill (and Werner)
and some great correspondents. However, one of my
fondest memories of Bill was spending time with him
in the Mt. Nimba forest in Liberia. It was part of an EIA
on a proposed mining concession, and it was just the
two of us for several days, which gave us plenty of time
for chewing the fat; especially when we talked about
rugby and Wales vs. South Africa or England, as I am
from Wales and Bill was originally from England, and
then South Africa. At that time, I had flown up from a
festival in South Africa and brought with me a ‘Green
Policemen’ helmet which Bill dually wore (Fig. 10, this
photograph shows Bill beaming a big smile).
Bill, I will miss you greatly—you were an inspiration
to me. Not only did you teach me a lot about reptiles, but
you were also a professional in everything else you did.
An expert and a gentleman. In the last communication I
received from Bill, a couple of months before he passed,
he told me ‘not to defer my dreams’—advice which is
applicable to us all and advice I intend to follow.
Michael F. Bates
Department of Herpetology,
Bloemfontein, South Africa
I knew about Bill soon after I started working at the
National Museum in Bloemfontein in 1983, as he was
then editor of the Herpetological Association of Africa’s
journal. The first time I met him was at the HAA’s first
National Museum,
Amphib. Reptile Conserv.
Fig. 11. Bill Branch in the Nimba forests close to Nimba
Mountain, Liberia (November 2011). Bill is wearing the
green policeman hat I had brought with me from South Africa
(Photo: Julian Bayliss).
conference held at Stellenbosch University in 1987. I
was only 25 at the time, and Bill was about 41, still quite
slim and with a full head of black hair! At that time he
was busy wrapping up work on the first edition of his
famous reptile field guide. Even then I remember Bill
having a certain charm about him and the aura of a man
with a deep knowledge of his subject matter.
Over the years I visited Port Elizabeth Museum
several times to examine specimens for various research
projects, including some on which I collaborated with
Bill. Having him all to myself and available to answer
my barrage of questions was always special. However,
I think my fondest memories were in the early 2010s
when we spent considerable amounts of time editing the
text for the Atlas and Red List of the Reptiles of South
Africa, Lesotho and Swaziland (published in 2014). As
first and second (Bill) editors, the bulk of the editing
fell on us. I would, for example, e-mail Bill the text
for a species account and ask such questions as “‘is it
still regarded as a subspecies” or “has anything been
published about this recently.” I could count on him to
respond within a day or two, and his responses were
always insightful. He seemed always to be up-to-date
with the latest taxonomy and the most recent literature.
And so it was that we e-mailed the various sections of
text back-and-forth until we were both happy. I have
very good memories of those times.
Another special memory I have of Bill was in May
2018, a few months after he was diagnosed with MND,
when I visited him at home in Port Elizabeth, together
with Aaron Bauer and Marius Burger. By this time he
was, for the most part, wheelchair-bound. Nevertheless,
he was as talkative and interesting as ever, especially with
regard to herpetological matters, and he also exhibited
his usual great sense of humour. We spent most of the
time at the computer in his study where he showed us
photographs of interesting and new reptiles, and of field
trips he had conducted with various colleagues over the
years. Also, I brought him a copy of a recent taxonomic
paper on egg-eating snakes (Bates & Broadley) that
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Tributes to William Roy Branch (1946-2018)
Fig. 12. Michael Bates (left) with Bill Branch and Darren
Pietersen during the Herpetological Association of Africa’s
conference in Pretoria in 2013 (Photo: W.R. Schmidt).
had just been published in the National Museum’s
journal Indago. The front cover of the journal featured a
montage of Bill’s excellent colour photographs of these
snakes, and it gave me great pleasure to see how pleased
he was with the way it turned out.
Bill had an enormous presence in the field of African
herpetology. He impressed me as a very well-read
man, and this was reflected in his wide and seemingly
limitless knowledge of reptiles and amphibians. Bill was
always willing to share PDFs of research articles and in
this way he helped me on innumerable occasions. Also,
I was inspired by his style of writing and attention to
detail. I still think about Bill often and will miss him for
several reasons, not least for the fact that his expertise
was always just an e-mail away.
Pedro Vaz Pinto
Kissama Foundation, Luanda, Angola & CIBIO-
InBIO, University of Porto, Portugal
I first met Bill in January 2009 in the most appropriate
of places: deep in the Angolan Namib desert, in
Iona National Park. We were part of a large group of
scientists assembled by Brian Huntley for a biodiversity
expedition in southern Angola. I remember approaching
Bill after dinner in the camp site, and he was keen to
see my photo files and became interested in some bush
viper pictures, which led to a few engaging stories and
discussions. At that point I was simply curious about
reptiles, and more involved with furry or feathered
creatures. The following day, I drove my Land Cruiser
to where I could see Bill and his colleagues had parked
their pick-up truck next to some granite boulders. I could
sense some excitement in the party, so I asked Bill what
they were doing. He invited me to join them and opened
a little box to retrieve a tiny beautiful little gecko, one
of the gems of Angolan herpetology which was not even
formally described at the time: the endemic Plume-
tailed Gecko, Kolekanus plumicaudus! He then showed
what was special and unique about that species and
chatted about other leaf-toed geckos. I was fascinated of
course, and it was quite an introduction to reptiles. Over
Amphib. Reptile Conserv.
Fig. 13. Bill Branch processing specimens in the fading light
of the Angolan Koakoveld (Photo: Pedro Vaz Pinto).
the following years we would become good friends, but
looking back I’m still amazed to realize how generous
he was by sharing that amazing find with someone he
had just met the previous day. Other scientists would
have kept their cards very close to the chest. But Bill
kindly drew me towards the world of herpetology for
which I’m forever indebted, but above all I believe
he made me a better scientist and better naturalist. He
taught me to make an effort at looking into the bigger
picture, to see the multiple layers and connections that
lie hidden behind the outer surface of a given ecological
theme.
My best memories with Bill, without any shadow of
doubt, were the days in which I was privileged enough
to travel with him to some of the most remote corners,
wildest places, and biodiversity hotspots in Angola.
We would typically look for a scenic landscape off the
beaten track and choose our camping spot. Some of
the time shared with Bill, around the campfire in the
Angolan desert, mountains, or forests, was memorable.
Our camping expeditions were hugely stimulating
scientifically, exciting and unpredictable, and very
importantly, always bathed by loads of good humor!
These expeditions could be physically exhausting, but
soon after I was looking forward for the next trip with
Bill.
Other scientists are much better prepared to praise
Bill’s unique and extraordinary legacy to African
herpetology. I can add that he did leave a crucial mark on
Angolan herpetology, but tragically with his premature
passing away, it wasn’t allowed to further crystalize
during his life. He was arguably the most influential
herpetologist to have worked in Angola for a sustained
period, and is the main person responsible for bringing
herpetology into the biodiversity agenda in modern
Angola. I have no doubt that his pioneering role will be
recognized in the future by young Angolan biologists.
On a personal note, whenever we came across a new
lizard or snake, I got used to my sons asking me ‘- Will
Bill want this specimen?’, ‘- Has Bill identified this
species?’, ‘- Does Bill need more specimens?’ and as
result, these now rhetorical questions remain quite vivid
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Conradie et al.
Pe
ws
Set
ge |
Sy S \ : —— oh. Sa age S-
Fig. 14. Bill Branch photographing a Jameson Mamba
Angola with Ninda Baptista (Photo: Pedro Vaz Pinto).
in
and still drive me on my searches. There are still a lot
of ‘goodies’ that we will catch for you Bill, and that’s
a promise!
Kirsty Kyle
KwaZulu-Natal, South Africa
I had the good fortune of growing up at Kosi Bay
with Bill Branch as a much loved family friend. Bill
had gotten to know my parents, who were the resident
scientist and his wife for the area. In those days, he did
an almost annual foray to Zululand, what with it being
such an interesting part of the country for herpetofauna.
Whenever he moved through the area, with his pack
of scientists, they would use our house as a base, and
for my two older brothers and I this was just the best
thing ever. His trips became the highlight of our year
and I think he thoroughly enjoyed having three young,
able-bodied slaves, ever so willing to dive after any
reptile that was silly enough to stick its nose out 1n our
vicinity. A friendly disagreement developed as we got
older and started objecting to his pickling tendencies.
In the later trips we would “not see” a lot of the more
common species because dear old Uncle Bill would just
pickle anything we presented him with, which was a bit
hard on our budding conservationist hearts. Although
we had a pretty much genetic interest in herps, I think
those times with Bill were extremely formative in all
three of our lives, they certainly were in mine. The fact
that he was interested and enthusiastic in teaching and
encouraging a little blonde thug of three years old in the
ways of reptiles was amazing.
Bill was absolutely instrumental in setting me on
the path I am on today. Throughout childhood it was
a privilege to spend time in the field with him and just
absorb all the information he so generously and freely
dished out. It had a major impact on my interest in
herps. I emailed back and forth with him whenever I
found something interesting, and I sent him pictures of
all sorts of different reptiles over the years and he would
always respond in his warm, friendly, and encouraging
manner, which was just amazing. My favourite memory
of Bill would have to be on his last visit a few years back,
Amphib. Reptile Conserv.
xi
when he proudly presented us with a beautiful pot that
Donvé had made, decorated with an aloe he informed
us he’d just plucked from our outdoor lizard enclosure.
There were no flies on Bill and I loved that about him,
he always told you the truth, even if it put him in not the
best of lights. We still have the aloe in the pot.
I wish I had a picture with him from the early days
because it really would be a cute one. I fondly remember
parking on his lap as a very little girl, discussing
whatever, feeling terribly important, with his black
mop of curls and my blonde mop of curls. It would
have been such a cute picture. I miss Uncle Bill, the
world in general is a lot less fun without him and my
Facebook is a much darker place without his frequent
updates, pictures, thought processes, and quips. I hope
he forgives me for specialising in amphibians instead of
reptiles, and I’m incredibly grateful to have had him as
a friend, as well as a mentor.
Krystal Tolley
South African National Biodiversity Institute, South
Africa
I knew about Bill before I moved to South Africa in
2001, as he and Colin Tilbury had some chameleon
DNA samples for my upcoming postdoc project. The
project almost didn’t happen, as Bill and Colin got cold
feet, but when I arrived I learned that they decided to
let me give it a try. Their trust in a stranger with whom
they had never worked ended up building a friendship
and collaboration that lasted nearly two decades. As
that project progressed and more projects arose, Bill
encouraged and supported me both in a personal and a
professional capacity. In fact, the entire herpetological
community welcomed me, something that I was not used
to, coming from the competitive world of marine biology
in the northern hemisphere. Because of Bill, Colin and
all the SA herpers, I felt like I had found a home that I
didn’t want to leave, and Bill was instrumental in that.
I cannot remember actually meeting Bill for the first
time. My first distinct memories of hanging out with
Bill and all the herpers is from the Port Elizabeth HAA
conference in 2004. What sticks out in my mind 1s that
at the concluding banquet, Bill received the Exceptional
Contribution to African Herpetology Award and he was
so touched by this that he wept. That spoke to his nature
as a caring person who knew that strength and courage,
not weakness, comes from personal relationships
and bonds. And his connections with his friends are
something he fostered.
I have many distinct and fond memories of Bill but
strangely enough, most of them relate to our friendship,
not to herpetology. When we would meet, the first
things he would ask me about was how I was, how was
my personal life, what was happening, was I happy?
He had many wise words for me along those lines,
giving advice, encouragement, and reassurances that
eventually I would find my path. Then of course, the
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Tributes to William Roy Branch (1946-2018)
‘herp talking’ would start. He would go on for hours,
non-stop, about snakes mainly. Most times, the topics
were just beyond me. I tried to absorb what he said, but
there was so much information that my brain couldn’t
handle it. I do remember that a long discussion about
Leptotyphlops made me realise what cool things they
are, and I still hope one day to actually work on them.
I was fortunate to have the chance to visit Bill shortly
before he passed away. We both knew, as did his wife
Donveée, that I was there to say a final goodbye. This was
indeed the last time I saw him and it was emotional for
everyone, but my memory is still a good one. The same
old routine was there. He asked me about my life first,
and he gave me wise words and insight about life. Then
he spoke about herps (including Leptotyphlops) for
about four hours non-stop. The thing that was different
this time, was that he often interjected the conversation
with things about himself. Dreams and wishes, failures,
successes, lost opportunities. He talked a lot about how
it’s important not to waste time on petty or destructive
things in life. But to focus time and energy on the people
in your life that care about you and to never take that for
granted. He spoke about the balance between the work
related passions of a herpetologist, and that this has to
balance with life, friends, and family. Bill was a hard
worker, but he did focus on family and friends, and I don’t
think he took any of that for granted. The way that his
first questions always related to our personal connection
and friendship, and about which analysis I was running,
speaks to that. The wisest words that Bill ever said to me
are: “Friendship 1s a gift. It’s a gift that others chose to
give, and that you chose to accept in whatever form it
takes.” Bill gave that gift to me and to so many others.
That is what I will remember him for the most.
Fig. 15. Bill Branch and Krystal Tolley in south-western
Angola in 2009 (Photo: Krystal Tolley).
Mzi Mahola
South Africa
I first met Bill when he arrived at the Museum. A year
or two later, I invited him to join our Port Elizabeth Mu-
seum soccer team, which was playing in the Industrial
League. He didn’t play many matches, because of his
Amphib. Reptile Conserv.
xii
commitments, but he was a good soccer player. A year
later, I was transferred from my department to join and
work with him as his research assistant. We often went
to Sardinia Downs to tag, study, and monitor the move-
ments, growth, and development of tortoises. After that
he introduced me into his other research and study pro-
gramme of other animals, such as frogs, snakes, and liz-
ards.
One day we were going up the Zuurberg Mountains
when he made a deal for us; “If you happen to catch a
snake first, I will buy you a bottle of beer at the Zuur-
berg Inn on the way back; but if I make the first catch,
you will buy me a bottle.” That was fair enough for me.
Bill was at the wheel of our Land Rover. We were driv-
ing towards the forest at the foot of the mountain when
I saw a female boomslang flying towards the forest. Bill
noticed my hasty intention to open the door of the mov-
ing vehicle and he quietly said, “Forget it! Boomslangs
are very shy; you'll never catch it unless it is ina tree.” A
few minutes afterwards, we left the Land Rover and with
our hunting gear and went our separate ways. It took me
less than five minutes before I heard the hissing sound of
a slithering snake. I saw the disappearing tail of a rinkals
entering a hole amongst rocks on a ledge. I put on my
safety glasses and peeped into the hole, and saw the two
shiny eyes watching the entrance. With my tools I pulled
the snake out and put it in my canvas bag, and declared
my victory to Bill. He didn’t believe me. It didn’t matter
how many snakes he collected afterwards. I had beaten
my master in his game and the bottle of beer would be a
cherry on top.
We were on a trip to the Drakensburg Mountains and
our first night stopover was in Centane, at my in-laws. We
shared the same bedroom. At night, Bill said something,
which I could not let pass unchallenged; “Kentani is the
only place, in the Eastern Cape, that has no tortoises.”
“Why?” I asked, thinking that this had to do with the
climatic environment.
“Africans ate all of them and left nothing to sustain
these animals.”
“No! That is not true!” I protested, because I had a
relationship with these people.
“What do you mean, it is not true? Dr.... (/ dont re-
member his name) learnt about this when he was inves-
tigating the cause of their depletion in this area, years
back in the early twenties. I read his book and you can’t
dispute it.”
“Well, his assumption was wrong.” I replied, confi-
dently, knowing that what he was going to hear would
shock him. “First of all; it 1s very, very difficult for a
stranger to get information from traditional amaXhosa,
because these people are known for their scepticism of
strangers. If you ask them anything, they will ask, “why
do you want to know?’ After that they will not share with
you their knowledge; more so if you’re a stranger. In
the past amaXhosa trained their children from an early
age never to tell a stranger the truth, especially to white
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people.”
Bill listened quietly, without interrupting.
I continued, “Now let me tell you something that they
did not tell Dr.....? AmaXhosa did not eat any creeping
or crawling animals, like centipedes, lizards, snakes,
crabs, frogs, locusts, ants or tortoises, hence they looked
down upon Khoisan people, because of their “repulsive”
diet. The Khoisans ate these animals.
Even though they were converted into Christianity,
there are still some Xhosa households who hunt and kill
or keep tortoises for their strong religious or cultural be-
liefs. They generally believe that if they burn a tortoise
Shell in a kraal with cattle, the cattle will multiply. Cat-
tle are a status symbol or a bank to our people. Tortoise
shells are also used as troughs to store drinking water for
chickens so that they may increase. There is also a belief
that if live tortoises are kept in a household, they will
repel evil spirits. These beliefs surely must have been the
cause of depletion of these animals in an area as conser-
vative and traditional as Centane. I was told that because
of their scarcity, locals are prepared to purchase and im-
port them from other areas.”
“It makes sense,” Bill said and kept quiet for a long
time afterwards.
Working with Bill had a very strong impact on me. He
was very dedicated and committed in whatever he was
doing. In Matatiele, he went out into the night to search
for frogs in the river while it was raining and thundering.
He didn’t allow anything to stand in his way. Many years
later, after I had left P. E. [Port Elizabeth] Museum, I
went on a personal and voluntary excursion of document-
ing and taking pictures of bushmen paintings in the caves
in the Nkonkobe and Chris Hani Municipalities. Without
his basic research training I wouldn’t have embarked on
this project. Bill gave me a hands-on experience in re-
searching and I thank him for sharing his skill with me.
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Fig. 16. Bill Branch discussing the finer points of the day’s
photographic record of collections with colleagues and
students, Lagoa Carumbo, May 2012. (Photo: Brian Huntley).
Amphib. Reptile Conserv.
Brian J. Huntley
South Africa
During 2009 and 2012 I had the pleasure of introducing
Bill Branch and a few dozen other field biologists to
the diversity of life in the deserts, montane grasslands,
miombo woodlands, forests, and floodplains of the far
reaches of Angola. Bill soon proved to be the hardest
working and most convivial member of the teams, which
comprised up to 30 biologists from ten countries.
During the first expedition to southwestern Angola,
in January 2009, we camped out on the Humpata
highlands and in the Namib desert. Here Bill and fellow
herpetologists found multiple new records and several
new species of frogs and lizards. From the faint light
of dawn to the pitch darkness of night Bill would be
in the field or at the makeshift laboratory tent, where a
generous donation of Cuca beer from the local brewery
kept spirits and laughter levels high. What impressed me
most about Bill was his ability to inspire all around him—
young students to ageing professors—game rangers to
army generals—with fascinating stories about his cold-
blooded friends.
In May 2012, when we were camped out along a
Congo tributary at Lagoa Carumbo, in the far northeast
of Angola, the evening’s discussions around the campfire
ranged from Bill’s erudite interpretation of current species
concepts to scary personal experiences of snake bites and
the treatment thereof. We were eight hours drive from
the closest town, and another five hours from the closest
doctor. One afternoon, Bill had been out to set a trap for
a black mamba that had been seen slithering down a hole
on arock face. He casually told us how he had, that same
morning, pulled what he thought was a harmless water
snake out of the Luele River. Only when he returned to
camp did he discover that it was a new elapid record for
Angola — Banded Water Cobra, Naja annulata.
We had planned to visit Portugal together early in 2018
to discuss collaborative projects with colleagues at the
University of Porto, but at a meeting in Cape Town that
January, Bill informed me of the advice his doctor had
given him that week: he should not travel. We soon learnt
of the severity of his illness, but this did not slow Bill
down. He was already under heavy pressure to complete
his catalogue of Snakes of Angola, but did not hesitate
to honour his promise of a chapter on reptiles for the
synthesis volume that I was coordinating on Biodiversity
of Angola. We kept up a lively correspondence to the
end, his sharp wit never failing. Fittingly, given Bill’s
tremendous role in inspiring young researchers in Angola,
the synthesis volume includes a dedication to him.
Roger Bills
South African Institute for Aquatic Biodiversity, South
Africa
I first met Bill in Marromeu, central Mozambique. We
were part of a team lead by Jonathan Timberlake looking
at the biota of the lower Zambezi’s delta region. I had
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
driven up from Grahamstown with a bakkie and trailer,
and had slept in the car over several nights due to poor
road conditions and slow progress. Basically, I was
exhausted. This did not get me any respite from Bill’s
sharp humour and I had to quickly shape up.
For me the trip was tremendous—there was water
everywhere despite it being the dry season, and an
abundance of fishes and the fauna was mostly new to
me. For most of the other zoologists 1t was not the best
season and consequently a bit frustrating. Bill and I got
on from the start and we spent time out in the dry fields
with a large bulldozer that was flattening termite mounds
looking for snakes and lungfishes and several days on a
boat going down the Zambezi.
The boat trip down the Zambezi was supposed to be
an overnight affair—down the Zambezi to the mouth, a
channel through mangroves to one of the delta’s southern
braids and up to the small village of Malingapanzi.
Unfortunately we missed the tide and left late, and went
down river on an incoming tide. It took us the whole
day to get down to the mouth where we camped at a
fishing village overnight. We expected to get going at
first light but the local fishermen stole our rudder as they
wanted payment for camping. It took our Mozambique
counterparts the whole morning of negotiating and
refitting the rudder before we could leave. The time
however was well spent: Bill went fishing (he was a good
angler) and caught our only Glossogobius giuris for the
trip, and I caught a load of mud-skippers in the mangrove
flats. Our delay meant we missed the tide again and going
up the southern channel to Malingapanzi was against the
outgoing tide. We got there late on the second day—Bill
had caught one puff adder. He wasn’t very happy and did
not return by boat the following day.
From all my experiences with Bill, the impressive
thing about him was his resourcefulness in the field,
whether collecting by himself or soliciting samples from
locals, he managed to get incredible numbers of samples.
Returning to camps in the evenings would invariably find
Bill at a table covered with specimens that he would be
fixing, photographing and taking tissue samples from. He
Fig. 17. Bill and Anton Bok at the Kalumbila Mine Camp,
Mwinilunga District, North-West Province, Zambia, May 2010
(Photo: Roger Bills).
Amphib. Reptile Conserv.
spent long hours doing this work. On one trip to a sand
mining project near Pebane, Mozambique, we fell afoul
of this. Bill had been there the week before and the locals
were used to giving reptiles they had caught to passing
vehicles. On our drive from the airstrip to the exploration
camp we were oblivious of this. After the second snake
came through the window in a flimsy plastic bag, we
wound up our windows and did not stop anymore!
Bill was an incredible intellect, a world-class scientist
but far more importantly a great guy. It was a privilege to
have spent time with him, my life 1s richer for it.
Johan Marais
African Snakebite Institute, South Africa
Back in 1980, while I was curator of Transvaal Snake
Park, I met Bill during one of his visits but we barely
spoke. I was a youngster cleaning snake cages and Bill
was visiting Rod Patterson and Anthony Bannister. We
often corresponded and I supplied Bill with a bunch of
photographs for his field guide, but it was only in early
2000, on a field trip to Namibia, that we really bonded.
We did several field trips to Namibia, often with Aaron
Bauer, but our trips to Niassa in northern Mozambique,
Mulanje Mountain in Malawi, and southern Angola
were memorable. Field trips are special as there 1s ample
time to chat, especially when driving long distances. I
particularly enjoyed the chats with both Aaron and Bill,
and although there were endless topics discussed it
was largely about reptiles. I often wound Bill up about
photographing reptiles on inappropriate props like fruit
and flowers that were out of place, and he accused me of
taking rather poor photographs as I had a bad eye.
His wry sense of humour brightened things up on
those long journeys and he was particularly good at
irritating Aaron, not to mention times when he would
lose specimens while photographing them! My best
Bill moment: when an American missionary’s wife
in Nampula asked Bill what he does for a living, he
responded that he was a reptile scientist who did field
work, described recently discovered reptiles, and wrote
scientific papers about his discoveries. She responded:
i Po, .
i —
Fig. 18. Johan Marais and Bill Branch with a Rock Monitor in
Namibia. (Photo: Jackie Childers).
September 2019 | Volume 13 | Number 2 | e186
Conradie et al.
“Yes but what is your real job?’
It is hard to grasp the gap that Bill has left behind, and
so many of us miss the times that we could call or drop
him an E-mail. He was notoriously bad at responding to
E-mails so I got into the habit of numbering my questions.
Needless to say, Bill would only answer those he felt like
answering.
Mark-Oliver Rédel
Museum fiir Naturkunde, Germany
My first contact with Bill was in 1996. He asked for a
copy of my frog book, and invited me to give a talk on
West African amphibians and reptiles on the third World
Congress of Herpetology in Prague, where I met him for
the first time in person. Bill was organizing a session to
summarize the progress in African herpetology. Thus, it
was Bill ‘officially’ introducing me, my Ph.D. not yet
finished, to the community of African herpetologists. We
kept contact thereafter, but it took a few years until we
met again.
Following a workshop to define conservation
priorities for West Africa, Conservation International
started a series of rapid biodiversity assessments in little
known areas across the Upper Guinea forests. In early
2002, Bill and I were asked to participate on one of these
RAPs, targeting the Haute Dodo and Cavally Forest
reserves in western Céte d’Ivoire. He was responsible
for the reptiles and I was to focus on amphibians, but
of course we conducted all field work together, recorded
many interesting amphibian and reptile species, ignored
all CI safety rules, and had a lot of fun catching animals
and talking rubbish. For Bill it was his first time being
in West Africa, and his first time working in rainforests
(as a ‘typical’ South African he showed up in shorts and
it took me quite a bit to convince him that working in a
rainforest in shorts is a very stupid idea).
Not all of the experiences were fun. In one night in the
Cavally forest, we walked far from camp and encountered
a few rarer species we hadn’t seen before on the trip. On
our way back, we stumbled straight into the largest raid
of army ants (Dorylus sp.) I ever encountered! The forest
floor and all lower parts of the shrubs and trees were
covered with these aggressive insects, and in seconds the
ants where everywhere on and under our clothes. We just
ran to leave them behind, and then had to strip naked to
pull off hundreds of ants, all holding onto the skin they
had successfully penetrated with their sharp mandibles. It
was only when we finally finished them all off (one has to
pinch off the heads of every single one) and turned again
towards the campsite, that Bill realized that he had lost
his glasses. We had to turn back into the ants to search for
them..... A much more pleasant experience on that trip
was when we found the first live caecilian, Geotrypetes
seraphini, Bill had ever seen.
Caecilians were also one of the most spectacular
findings, actually the first country record for the entire
group, the next time we met. In the fall of 2003, Bill
Amphib. Reptile Conserv.
XV
invited Johan Marais and I to survey amphibians
and reptiles in the Niassa Game Reserve, in northern
Mozambique. Although it was the core dry season it was
an extremely successful survey, revealing 57 reptile and
31 amphibian species, including a new Cordylus, and
further potentially undescribed species including the
Scolecomorphus mentioned above.
Thereafter we met regularly, mostly in South Africa,
but a few times in Germany as well. Bill often took me on
shorter excursions across southern Africa, e.g., showing
me spectacular parts of the Cape Fold Mountains or the
Karoo, and I frequently visited him and his wife Donvé
in their amazing house and garden in Port Elisabeth.
There we had long and entertaining discussions about
herpetology, science, politics, or sports, while sipping
on a nice glass of wine, observing the many birds in the
garden, or following a soccer or rugby match on television.
We never agreed on which soccer team or player was
worth supporting, and I could always bet that I would
receive a derisive email after a German defeat against
an English team in the Champions League. Bill was
mad about some sports and missing an important rugby
match was impossible, even on an excursion. Particularly
memorable was when we once drove through the Karoo
and he wanted to listen to a match on the radio. As the
radio quality was weak, we had to finally stop and follow
the broadcasting on the roadside in the desert. However,
the only program Bill could find was in Afrikaans. Thus
apart from the players’ names and the score, he did not
understand a single word. An amazing fact about Bill
was that, although he was a forceful speaker, loving
to use and to play with the English language, he was
completely ignorant about other languages. So he never
learned Afrikaans and in other countries, other people
had to cope with translations.
But Bill had encyclopedic knowledge of the natural
sciences in general, and he could instantly give a lecture
about southern African zoology, botany, or geology.
He was easily connecting all this different knowledge
into a broader, comprehensive framework and thereby
developing new questions and ideas. This ability to
communicate new or complex knowledge made him a
very stimulating academic teacher, something which was
certainly was one of the reasons why he was so popular
on the National Geographic tours he was guiding in his
later years. His non-protective way of openly sharing data
and ideas, as well as critically and without any mercy
dissecting project ideas, hopefully remains a model
to all the many students and colleagues with whom he
was communicating his entire life. Many of his ideas
and projects now remain to be finished by others, most
prominently the revision of the ‘bible’ Bill Branch’s Field
Guide to Snakes and other Reptiles of Southern Africa,
and the description of dozens of new reptile species he
had already collected and deposited in the herpetological
collection of the Port Elizabeth museum.
To me, Bill was much more than a good colleague,
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
Fig. 19. Bill Branch in a sad mood after his snake stick,
proudly stolen from Aaron Bauer, broke while he tried to
destroy an Opuntia in the Karoo, October 2012. Bill: “What an
embarrassing death to a snake stick, killed by a plant” (Photo:
Mark-Oliver Rédel).
although we did only meet occasionally. More often
in recent years, he was a very good friend with whom
I enjoyed discussing everything, not only science.
However, the scientific discussions with him were a
constant inspiration providing me with many, sometimes
unusual ideas on how to interpret data or set up new
projects. He introduced me to the African family of
herpetologists and to Mozambique; and I am proud that
I could introduce him to the West African herpetofauna
and rainforests, and even convinced him (sometimes)
that amphibians are not completely boring. For him, I
would have even loved to see England take the World
Cup in 2018. He died too early and in an unbelievably
Fig. 21. Bill Benen a Mark- Oliver Rodel wan the halite
of the species named in their honour (Photo: Frank Tillack).
Amphib. Reptile Conserv.
xvi
,
& |
¥,
Fig. 20. Bill Branch and Mark-Oliver Rédel in July 2018 in
Bill’s home in Port Elizabeth (Photo: Mark-Oliver Rédel).
cruel way. I am very happy that I could meet him one
last time, shortly before his death in PE. He will always
remain an unforgettable person and inspiration. His death
is a great personal and scientific loss, and my thoughts
are with his beloved wife Donvé and both their families.
Paul H. Skelton
Wild Bird Trust, National Geographic Okavango
Wilderness Project
When the National Geographic Okavango Wilderness
Project (NGOWP) was looking for key specialists to join
them on expeditions into the unexplored highlands of
Angola, Dr. Bill Branch was a first port of call. Bill was
attracted into the NGOWP as an established authority
of Southern African and Angolan herpetology, most
especially the reptiles. He joined the founding 2015
NGOWP Expedition as part of the 'land party.' He also
took part in the 2016 expedition, joining it after first
enjoying an extensive journey through the escarpment
reaches of Angola in the company of Dr. Pedro Vaz
Pinto. Prior to this, he had visited Angola on a number
of occasions, collecting and adding significantly to the
herpetofaunal knowledge of the country. His collecting
antics often drew curious onlookers, mostly children, who
would marvel at what wonders he would bring forth from
the ponds, rocks, and crevices. More significantly he both
encouraged and actively mentored younger hepetologists
currently active in Angola. These expeditions have
resulted in several potential new species, a number of
new species for Angola, and range extensions of many
others.
Bill was an old friend and colleague of some of us.
I personally met and knew Bill soon after he arrived in
South Africa, and was working for the Atomic Energy
Corporation outside Pretoria. On joiming the Port
Elizabeth Museum, we became good friends and he
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Conradie et al.
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joined me on at least two interesting expeditions that I
arranged primarily for fish sampling—one was along
the Lower Orange River, and the other was to Lesotho
in 1988. Bill had a'nose' for reptiles. I remember vividly
how he would relish the refreshment breaks on the
expedition as we travelled north across the karoo, in
order to sniff around the rocky kopjes and outcrops along
the way. He inevitably returned with a clutch of reptiles
in hand, all of which were unerringly shot with an elastic
band from the hand. And then there was the spitting
cobra, Naja nigricollis woodii, he caught by the tail on
crossing the road, after screeching to a halt and leaping
forth from the vehicle. As viewed from the vehicle,
behind it was an energetic spectacle in madness—born
out on arrival to realise that Bill had been spat in the eyes
by the enraged reptile and, whilst he was blinded and in
agony, was desperately directing his non-herpetological
colleagues in the niceties of bringing a canvass bag to
bear so he could insert the writhing beast. Needless to
say, he succeeded and managed to wash his eyes out
before he was permanently damaged. On the Lesotho
trip, Bill was his amazing self and not only displayed
his fly-fishing skills that I never knew he had, but also
showed me the cryptic, super-jawed, Maluti River Frog
(Amieta vertebralis) in its natural habitat. His calm
demeanour, bubbling humour, and all-round knowledge
in the field was always refreshing. Simply put, Bill was
a pleasure to have around. His scientific productivity and
achievements are of a top order. His passing was a great
loss to our project and to the community at large.
Aaron M. Bauer
Villanova University, USA
I met Bill in 1987, during my first trip to South Africa.
I had met with Alan Channing in San Francisco and he
had given me a list of all of the critical herpetologists and
institutions to visit in South Africa. After visits to Wulf
Haacke at the then Transvaal Museum and to FitzSimons
Snake Park in Durban, I made my way to Port Elizabeth
via Cradock. I phoned Bill on the way (from a post
office, remember no cell phones?) and he suggested that
my field assistant and I stay at the camping ground on
Amphib. Reptile Conserv.
Fig, 23. Bill Branch in Angola bean for ean: (Photo:
Alex Paullin).
Brookes Hill. A gale was blowing and we were soaked
to the bone, but the next morning Bill kindly showed
me around the Museum complex. Over the next day or
two he took me Bradypodion hunting in Happy Valley,
just down Beach Road from the Museum, showed me
the introduced Lygodactylus capensis on the guard rails
along the roads, and sent me off to Schoenmakerskop to
look for Acontias meleagris, Homoroselaps lacteus, and
other reptiles. Like everyone I met on that first trip, Bill
was a critical contact if I was intending to start working in
South Africa. By 1989, I was coming regularly, sometime
Fig. 24, Bill Branch in Angola with a dead on the road Vine
Snake (Photo: Alex Paullin).
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Tributes to William Roy Branch (1946-2018)
Fig. 25. “Uncle Bill” enjoying the adoration of the masses
(Marius Burger and Krystal Tolley) at the H.A.A. meeting in
Cape Town in 2011 (Photo: Aaron Bauer).
two or three times a year, and more often than not Bill
and I would go to the field together, starting a 30 year
personal and professional collaboration that influenced
all of my work in Africa as a whole.
I have very many fond memories of Bill. One was a
1990 trip to northern Namibia. I picked up Bill and drove
with him and two of my students to a farm in Kamanjab.
We stayed with the farm managers and had a wonderful
time. The collecting was spectacular and mostly new
to both me and Bill, who had not spent much time in
Namibia before this. Every day we found additional
species, in the end nearly 50 species on the farm alone,
and more between Kamanjab and Palmwag. Bill had
to leave before me and on his last night, after weeks
of the best warthog and gemsbok, we were promised
“something special,” which turned out to be a very old
and very gamey goat! The next day Bill and I left the
students and drove straight through to P.E. with only a
short stop for a nap. Our only music in the car was The
Greatest Hits of Elton John. On the trip we really got to
know one another, and we both got so sick of Elton John
that we couldn’t listen to his music for years.
Other fond memories are of our multi-year projects
in the Little Karoo and later the Richtersveld. In those
days there were very few visitors to the Richtersveld,
and Bill and I both enjoyed the solitude of the park,
evenings by the fire along the Orange River, and finding
two Bitis xeropaga only meters away from one another.
I can also mention a magical trip to the Kaokoveld along
with Johan Marais and my Villanova colleague, Todd
Jackman. We were in the bed of the Munutum River and
all of a sudden we were surrounded by a herd of giraffe.
Even Bill, always ready for the good photo opportunity,
was temporarily awestruck by the scene. I also spent
many memorable weeks with Bill in the States. One trip
was to the South Carolina coast just after a hurricane.
Despite some serious close calls with disaster, the loss
of one of Bill’s cameras, and hundreds of mosquito bites,
Bill was pleased to catch a baby alligator and to have
Amphib. Reptile Conserv.
had the chance to be in the field with Whit Gibbons, a
great herpetologist and ecologist, and an author whose
writings Bill admired. On another trip, we drove 10,000
km from coast to coast and back in the US with my
students and postdocs. At 3,700 m we saw a herd of
elk and Bill managed to get most of his body outside
of our moving van to get the perfect shot. I think all of
these fond memories are united by the common theme
of sharing with Bill the feeling of how lucky we are to
have a vocation we love and that lets us enjoy spectacular
animals in amazing places in the company of our friends.
Bill was the face of South African herpetology, indeed
of African herpetology. His interests were wide-ranging
and he had a mind for details when it came to all things
herpetological. He was also a master naturalist who knew
his birds and his plants, as well as the history of natural
history exploration in Africa. He was also down-to-earth.
Even the most novice of herpetologists was welcome to
call him Bill, not Dr. Branch. Although he could, and often
did, go on for hours about something in a quite serious
tone, anyone who spent much time with Bill knew that
he had a wicked sense of humor, and conversations with
him could swing between debates about the International
Code of Zoological Nomenclature one minute to a
hectic exchange of friendly insults the next. That he was
known as “Uncle Bill” to many speaks volumes about
how comfortable we all felt with Bill. My relationship
with him was somewhat different. Years ago I told Bill
that I thought of him as the older brother I never had and
indeed, the last words Bill spoke to me were “Be well,
little brother.” We are all both better herpetololgists and
better people for having known Bill.
Stephen Spawls
Although Bill and I had corresponded since the early
1980’s, we didn’t meet until 1987, when Bill drove up
to Botswana and stayed a few days with us at Moeding
College, Otse. It was an exciting visit. Bill came in a
white windowless Volkswagen Kombi, which was the
same type of vehicle that had been used by the South
Africa Defence Force on their 1985 raid into Botswana.
Consequently, the Botswana security forces had tracked
the vehicle, and as Bill drove out of our college he was
stopped by the soldiers, who went through the vehicle.
Finding nothing, the military concluded that Bill had
cached his weapons at my house which was then
searched! After this inauspicious start, my wife and I
subsequently stayed with Bill in Port Elizabeth. We went
on an amazing safari, to the Addo Elephant National
Park, to Graaff-Reinet, and thence into the Karroo, where
we stayed at the Karroo National Park headquarters with
Bill’s friend, the warden Harold Braack. We returned via
the Swartberg and Oudtshoorn.
Being in the field with Bill in some of his favourite
country was an amazing experience; he knew the land, the
customs, and the animals, and gave freely of his expertise.
We found many spectacular species that were totally
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new to me, including Hewitt’s Ghost Frog, Heleophryne
hewitti, the Giant Ground Gecko, Chondrodactylus
angulifer, and the Blue-spotted Girdled Lizard, Ninurta
coeruleopunctatus. But we weren’t lucky all the time. At
one point Bill and I drove for several hours at night on the
tarred road near Beaufort West, hoping to find a Horned
Adder, Bitis caudalis, but we saw virtually nothing. As
we returned to the park, near midnight, there on the road
was a snake, and we leapt out with great excitement but
it turned out to be only a Herald Snake, Crotaphopeltis
hotamboeia. One morning Bill and I were pursuing a sand
lizard, Pedioplanis, which was sheltering 1n a clump of
bush. As it appeared near my feet I dove at it but missed,
and it fled to another clump. Bill clapped his hands on his
head. ‘It’s obvious you’ve always collected by yourself’,
he said exasperatedly, ‘you should have just shuffled it
towards me, not leapt at it without telling me.’
On that trip, we also learnt of each other’s shared
enthusiasm for bird-watching. As we drove across
country, Bill directed me to a side road. ‘I’ve got a
surprise for you,’ he told me, as we took the diversion.
We went a few miles and then Bill told me to pull up and
get my binoculars; and there, in a grassy area below the
road, were a pair of Blue Cranes, the first I had ever seen.
In 1991, I went to work in Ethiopia, and Bill wrote
to me in 1992, suggesting we might work together on
a book on Africa’s dangerous snakes. Blandford Press
showed interest in the project, and in 1993 Bill came
and spent a few weeks with us in Ethiopia, doing field
work and working on the book. We made several field
trips, one was to the highlands east of the Rift Valley,
to a town called Dodolla where a specimen of Bitis
parviocula, the spectacular Ethiopian Mountain Viper,
had been collected, still the only specimen known from
east of the rift valley. As we ascended the rift valley
wall, up through dense broad-leafed forest, we became
increasingly excited; this looked like Bitis parviocula
country. Then as we approached Dodolla, we emerged on
the plateau, and found ourselves on a vast open grassland,
as bald as a billiard table. Bill sighed and looked at me.
‘Listen, matey’ he said (Bill and I were both born in
North London, he at Finsbury Park, me in Muswell Hill,
and sometimes in the field we were just two Londoners
together), ‘we’re looking for a forest viper, and as far
as habitat goes, we’ve just gone from the sublime to the
ridiculous.’ But that day we did find some spectacular
frogs, including Paracassina kounhiensis, Mocquard’s
Mountain Kassina.
The following week, down in Awash National Park,
we had some remarkable luck; in one afternoon and
evening we got a North-east African Carpet Viper (Echis
pyramidum) under a rock right outside our room, on
the road in the dark we found a Kenya Sand Boa and
two species of egg-eater, and as we drove back to the
lodge, we caught a huge Atractaspis fallax on the road,
an adventure that Bill described as being ‘like trying to
subdue a spiked manhole cover.’ At Lake Langano, we
Amphib. Reptile Conserv.
xix
caught a small Egyptian Cobra (Naja haje) on the road.
Back in Addis Ababa, I was teaching one morning and
Bill worked in the garden, creating a small set on top
of a rather nice garden table to photograph the cobra.
Unfortunately, he incorporated several biggish rocks
in the set and in moving these around, he managed to
thoroughly gouge the polished surface of the table. My
wife went ballistic, but Bill turned on the charm and
managed to persuade her that it was all part of the great
scientific endeavour, and he took us out for a meal as
well. The following day I found Bill crawling around in
the canna lilies when I got home; one of the frogs he
was photographing had sprung into the flowerbed and
escaped.
We didn’t always get on well. Bill had a very relaxed
attitude towards deadlines, and often preferred to go into
the field rather than knuckle down. He once told me how
his publishers (Struik) ‘had flown him to Cape Town’
to finish his field guide, and a fellow herpetologist,
who overheard this, said ‘What you mean, Bill, is that
Struik made you fly there, sat you down in their offices
and said you weren’t leaving until you got it finished.’
Bill laughed and admitted it; and in one of his books he
thanks his editor for ‘making ridiculous deadlines seem
acceptable.’ Our work on the Dangerous Snakes of Africa
book was complicated. Bill was in South Africa, I was in
Ethiopia, and there was no e-mail in those days. We used
to send stuff to each other by courier. As the deadline
for the delivery of the manuscript approached, Bill had a
lot of the snakebite stuff still to do and wasn’t getting it
done. With two weeks to go and the publishers muttering
angrily about penalty clauses (the production was
catalogued, and tied into a publicity/release schedule), I
rang Port Elizabeth to be told that ‘Dr. Branch had left on
an extended safari to Zambia, and would not be back for a
few weeks.’ In a panic, I managed to get hold of Dr. Colin
Tilbury, who stepped into the breach and wrote virtually
all the snakebite stuff in short order. The manuscript went
in on time, but it led to a furious row between Bill and I
over the order of our names on the cover. But eventually
we got over it, and in fact in 2017, we agreed to do a
revision of the Dangerous Snakes book.
The last time I met Bill was in 2014, in Bagamoyo,
Tanzania, where we were part of a team assessing
Tanzania’s reptile biodiversity. We went out one evening
and I climbed a tree to catch a sleeping Spotted Bush
Snake. Bill watched thoughtfully. ‘I’m past climbing
trees’, he told me. ‘In fact, ’'m past climbing over
anything. Last time I was in Namibia with Aaron Bauer,
a lizard ran under quite a low fence and neither Aaron
nor I could get over it.’ He laughed, ‘It’s my fondness
for prawn curry.’ On that conference, Bill talked with
great enthusiasm of a projected book. ‘I really want to do
a big book’ he told me, ‘covering the natural history of
Africa’s snakes, along the lines of Harry Greene’s book.’
He showed me some ideas and pictures on his computer;
his ideas were mind-stretching and holistic; he saw
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
Fig. 26. Bill Branch photographing some lilies at Lake
Langanao, Ethiopia (Photo: Steven Spaw!ls).
the snakes in the landscape as part of the interlocking
whole ecosystem, and his accompanying pictures were,
as always with Bill’s photographs, spectacular. Nobody
else has photographed the African herpetofauna like Bill.
We started work on the revision of the Dangerous
Snakes book in early 2017. Bill sent me some draft
material, a list of important references (he had an
encyclopaedic knowledge of the literature on African
reptiles), and a stunning portfolio of pictures. But in
late 2017, Bill cautiously wrote to tell me he was having
mobility issues, and wasn’t sure how this might affect
our project. And in early 2018, to my shock, I heard
from Bill that he had been diagnosed with motor neurone
disease. But he remained full of optimism; and said that
he fully intended to do his bit; cheerfully pointing out
that Stephen Hawking had lasted many years with the
same affliction. But it was not to be. The disease quickly
took hold. Tragically, Bill died on the 14th October
2018. His untimely death is a major loss to African
herpetology. And I hope that our book, which should be
published in mid-2020, will be a suitable monument to
Bill. Few herpetologists have reached both the public and
their fellow scientists with such verve and accuracy as
Bill did.
Ss
Se Sc] Miisieees eos eS aa
Fig. 28. Bill Branch and others at Bagamoyo, Tanzania, in 2014.
Amphib. Reptile Conserv.
Fig. 27. Bill Branch admiring an old tank near Dodolla,
Ethiopia (Photo: Steven Spawls).
Andrew Turner
CapeNature, Western Cape, South Africa
I first met Bill Branch at an HAA meeting, I think the
Stellenbosch meeting of 1998 or thereabouts. He was the
top South African herpetologist in my mind because of
his comprehensive treatment of the reptiles of the region
(his lesser interest in amphibians did not bother me, as
his emphasis on the snakes more than made up for this).
He was always interested in other people’s experiences,
especially regarding observations on distributional
occurrence, and encouraged documenting this valuable
form of data. Knowing that someone like Bill, who
came from a rather different background, could switch
to making a career of herpetology—and a rather exciting
and enjoyable career at that—was a great inspiration for
me to continue my professional herpetological interest.
His photography was also inspirational and keeps me
(and many others) clicking away.
Bill was a great raconteur, and his stories of herping
gone wrong were particularly amusing. One story
in particular, although I don’t remember that exact
mechanics of it, involved Bill trying to catch a Cordylus
under a rock that was being lifted by a colleague. (I shall
not mention his name but he did have an extensive snake
collection at one point). Bill shoots his right hand under
the rock to catch the Cordylus but notices at the same
time there is a second Cordylus under the rock so shoots
in his left hand too, catching both of them. But then a
third Cordylus runs out from under the rock and said
colleague catches that one by dropping the rock on both
Bills hands!
Bill really set the scene for getting the full picture of
South African herpetological diversity, and did a good
job of placing this in an African and global context. He
travelled widely and shared his great photographs, and
was always wondering how the various species fitted
together. His fondness for the small adders was totally
understandable, and he did a good job of discerning their
subtle (and probably recent) divergence and highlighting
the need for conservation of several of these species.
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eo . = = Sp a h °
Fig. 29. Bill doing what he did best: geeing everyone up to
maximise income from the HAA auction! (Photo: Andrew
Turner).
Ernst H.W. Baard
CapeNature, Western Cape, South Africa
My career as a herpetologist with CapeNature (then Cape
Department of Nature and Environmental Conservation)
started in January 1983. My first task was to sort out
and process a few thousand specimens of frogs, lizards,
snakes, and tortoises collected and collated by my
predecessor, John Comrie Greig (Greig and Burdett,
1976. Patterns in the Distribution of Southern African
Terrestrial Tortoises) and, at the time, colleagues,
Richard Boycott and Atherton de Villiers.
After writing (yes, there were no emails those years)
to the curator of the Port Elizabeth Museum, Dr. Bill
Branch, and the curator of herpetology at the South
African Museum in Cape Town, Dr. Geoff McLachlan,
about depositing the specimens (roughly divided into the
Western and Eastern Cape), we got positive responses
from both curators. Atherton and myself proceeded, and
we completed the task of sending, among others, the
whole Greig and Burdet wet and dry tortoise collection,
and several hundred “eastern” Cape lizards, snakes,
and frogs to Bill at the Port Elizabeth Museum. Bill’s
epic paper on the lizards of the Cape Province (Branch,
William. 1981. An Annotated Checklist of the Lizards
of the Cape Province) made a huge impact on my
knowledge of the lizards of the Cape, and together with
FitzSimons 1943 (Lizards of South Africa) guided us
through the process.
An incident that stood out during this time, was
the discovery in the Jonkershoek collection of an un-
identified many-spotted lizard in a small bottle, collected
in 1973. It was beautifully preserved and, fortunately,
with a geographical location in the Groot Winterhoek
Mounatins down to seconds South and East (this was
before GPS). It took me a few days using FitzSimons
1943 to identify the lizard as “Lacerta” australis, and we
were very excited about this discovery. One unsuccessful
collection trip to the locality (by Boycott, De Villiers, and
Baard) was undertaken in February 1983, followed by
Atherton and I managing to collect two more specimens
Amphib. Reptile Conserv.
at the same locality in April 1983. Imagine our joy, since
these were as far as we could establish, only the 6th and
7th specimens known to herpetology of this “elusive”
species. This information was shared with Bill and he
encouraged us to publish a note which we promptly
did, asking him to co-author (De Villiers, Baard and
Branch. 1983. ‘Lacerta’ australis: additional material).
Bill was always supportive of any further investigations
and readily responded to queries on the herpetological
collection.
In later years, Bill got back to us and was very excited
about some of the tortoise specimens we sent him,
including some of the largest individuals of some species
he had encountered. He then published a short note in the
Journal at the time, honouring Atherton and I with co-
authorship (Branch, Baard and De Villiers. 1990. Some
exceptionally large Southern African chelonians).
I only met Bill for the first time at my first HAA
Conference in Stellenbosch a year or two later, and was
really honoured to make his acquaintance. His paper on
angulate tortoise ecology in the Eastern Cape (Branch
1984. Preliminary observations on the ecology of the
Angulate Tortoise) had a huge impact on my career,
since this paper shaped my thoughts and guided my
research and attempts at understanding the ecology of the
geometric tortoise of the Western Cape; having completed
my research in 1990. For a young herpetologist like me at
the time, it was almost natural to think: What would Bill
do in this case? or How would Bill approach this topic?
Bill’s astonishing knowledge of lizards, tortoises
and snakes, snake venom, snakebite, etc. was really
something to behold, and few herpetologists could keep
up with him. I fondly remember Bill at conferences
communicating with all and sharing his knowledge. The
best story I remember him telling, was about the evening
in the veld around the fire. After Marius Burger latched
a Pseudocordylus crag lizard to his (Marius’) earlobe,
Bill kept on touching the lizard which wouldn’t let go
of Marius’ ear; with the lizard biting down harder and
harder, Bill spent an hour or so enjoying Marius’ agony
and futile attempts to get the lizard to let go of his ear!
William R. (Bill) Branch was a legend of his
generation and time. Not only was he a brilliant scientist,
excellent herpetologist, and I believe, a great bird
enthusiast, but also somebody one could look up to. His
contribution to South African and global herpetology
will go down in history as exceptional, ground-breaking,
and outstanding, and will stand the test of time like with
other greats; FitzSimons, Broadley, etc. His contribution
to the written and peer-reviewed herpetological science
and popular literature is unsurpassed, and it is my honour
to have known him.
Amber Jackson
Cape Town, South Africa
Uncle Bill’s Bible was a well-used field guide by the
time I met the man himself. I had even sent him a few
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
Fig. 30. DNA sampling of Spek’s Hinged Tortoise, Kinixys
spekii (Photo: Amber Jackson).
specimens of Leptotyphlops years before when I was
a student. I finally met Bill as an awe struck herpie
requesting he sign my copy of his field guide before a
very serious meeting at my new place of work. He wrote:
“Wow, Uncle Bills bible!!! 167 species out of date, but
what else is there.” Out of nowhere he then spouted a
lecture about the Galapagos and island biogeography,
and held up the meeting for 20 minutes in the process.
All eyes on me, I left with my signed copy and some
knowledge I never requested but was all the better for
knowing. Little did I know, our first meeting was an
accurate precursor for the years that followed. Thanks
to numerous development EIA’s Bill and I travelled to
Lesotho, Augrabies, and Mozambique (multiple times),
with me always as his self-proclaimed assistant.
One of my favourite memories with Bill is lying in
the dark, on a rocky shelf at the top of the Augrabies
paleo falls, staring at the stars and waiting for the
geckos to come back out after our disturbance. The stars
were incredible! I later caught him a Pachydactulus
atorquatus, without breaking the skin, and received an
exclamation of ‘I could kiss you.’ He didn’t, and ran off
with his prize. At the time, I was naively more excited
that 1t meant we could go to bed before our dawn wakeup
call in four hours. Bill, 40 years my senior, put me to
shame with his energy levels.
We got along at first because I was eager to learn,
and he was eager to teach. Then one day, I called him
a bastard for one of the anti-feminist comments he used
to purposefully provoke me with, to which he laughed,
Amphib. Reptile Conserv.
Fig. 31. Bill reading science in 45 °C heat (Photo: Amber
Jackson).
sighed, and said “finally!” All pretenses over with, we
were then friends.
Most of my time with Bill was spent learning, so
much so that my brain stopped being able to absorb
any more information and saturated by the end of the
long day. The knowledge he possessed was impressive,
diverse, and felt insurmountable. He taught me plenty
about herpetology and science in general. His enthusiasm
was contagious and witnessing his studiousness in the
field was impressive, with his daily diary and specimen
processing. But one thing that stands out is the things he
probably never intended to teach me, for example: How
being reserved doesn’t have to impact negatively on your
life, how euthanizing something as cute as a bush baby
can make a huge contribution to science and someone’s
career, or how LED lights can make fresh produce more
appealing. How just because your life starts in one place
doesn’t mean you have to stay there. How you can be a
jack of all trades and a master of one. How you can make
mistakes. That apologies are important. How careers can
be diverse and often unfold. That one of the biggest joys
is to love, freely and openly.
To the man that “was by turns (and somehow all at
once) relaxed, intense, sincere, self-mocking, modest,
confident, serious, and funny.” Kim Stanley Robinson
To the man that could make an economist understand
biodiversity by using economic terms.
To the man that could answer the question: “Is a
penguin a fish or a bird?” politely and honestly.
To the man that could provoke an entire lecture with a
simple question: ‘What’s the odd one out?’
To the man that believed in love, in science and in the
unknown.
To the man that studied cancer but fell in love with a
cobra while fishing.
To kind, funny, and sometimes forgetful ‘Bum in the
Butter’ Bill.
I think about you often, your teachings, your adventures,
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Fig. 32. Bill with a shoftshell terrapin he caught (Photo: Craig
Weatherby).
¥ fe a! 7h? 7
ov ; / ak d a
our last day together, and all the days before then. I couldn’t
have asked for a better mentor, teacher, and dearest friend.
I will treasure you always. Thank you for believing in me.
Margaretha Hofmeyr
University of the Western Cape, South Africa
I first met Bill Branch in October 2000, when my
colleague Alan Channing invited him along on a field trip
to Namibia for the UWC Zoology Honours students. I had
most students with me in my husband’s Kombi Synchro,
while Bill was a passenger in Alan’s Land Rover. We
stopped at Springbok’s Caravan Park for the first night,
where I booked accommodation in chalets. Because Bill
joined the party at the last minute, I knew there would not
be a bed for him and had some concerns about sleeping
arrangements. For one or other reason, perhaps because
Bill was idolised by all herpetologists, I expected him to
be rather arrogant, but he quickly won me over when he
made a bed for himself in the trailer Alan took along. The
trailer was quite short, but so was Bill; fortunately the
trailer was rather wide, because so was Bill. The sight of
him surfacing the next morning from his trailer bed will
always stay with me. Yes, he might have been arrogant
at times, but he was always a great sport, and teased the
students to distraction on this trip.
I always feel dishonest calling myself a herpetologist,
because my field of expertise is restricted to tortoises
and terrapins. Yet, on this trip, as herpetologists do, we
went on night drives to look for herps (never tortoises)
on the roads. One of the nights while staying at Klein
Aus, everybody squeezed into my Kombi to search for
exciting things on the roads. While driving through a
narrow stretch of road between two fences, a springbok
ram materialised in the road before my husband’s car. I
switched the main lights off within seconds, but it was
still too late. The springbok ran straight into the Kombi,
broke his neck, and put quite a dent into the front of the
car. All the girls were crying but we had to deal with the
situation. Alan and Bill dragged the springbok out of
the road and then we had the unfortunate task of driving
to the owner’s house to report the incident. His only
Amphib. Reptile Conserv.
reaction was that it was the only springbok he had on
the farm. This was an unpleasant experience for all of us
but also created a bond, because Bill mentioned it many
times to me in ensuing years.
At conferences, I would get annoyed with fellow
herpetologists for teasing Bill about his lisp, yet, he
always laughed at their jokes. To me, the ability to laugh
at yourself reflects true character, and Bill had that. I have
many fond memories of Bill and always regarded him as
the ultimate herpetologist and naturalist in South Africa.
His expertise stretched so much wider than reptiles and
amphibians. He may not have been an expert on every
animal or herp group, but his knowledge was astounding.
He was also willing to share his expertise and helped
many young scientists to find their way. I may not be
described as a young scientist, but when I switched from
large mammals to tortoises, Bill knew much more than I
did, and he was willing to share. Over the years we co-
authored several papers and it was always a pleasure to
work with him in a professional capacity. South Africa,
Africa and the World are now deprived of one of their
top intellectuals, and an exceptional person—we salute
you Bill.
Jens Reissig
Ultimate Creatures, Gauteng, South Africa
The first time I met Bill was during a high school field trip
to northern KwaZulu-Natal around the year 2000. At that
stage, I was rather shy and having had a very keen interest in
reptiles since my early childhood I of course knew exactly
who he was, however never made any contact with him.
Many years had passed until I crossed paths with him again
at the Herpetological Association of Africa’s Conference at
the National Zoological Gardens in Pretoria, South Africa.
From this point on, we stayed in contact and he was always
willing to help wherever he could. Unfortunately, he was
extremely busy while I was compiling my book on the
Girdled Lizards and their Relatives in 2013 and 2014, so
that he was not able to assist me with it in any way. He
did however end up reviewing the book for me. The book
review ended up being published in Herpetological Review,
2015, 46(2): 1-7.
After having received the tragic news of Bill’s
diagnosis, I decided to go and visit him at his home in
Port Elizabeth on the 20th of April 2018. Even though
one could see that he was battling his illness, he still tried
to be upbeat about life and could not stop talking about
reptiles and a (to me) hidden passion of his, Orchids. We
sat for hours on his patio talking about various reptile
projects, his Orchid collection, birding, and some of his
many field trips into Africa. After spending quite some
time with us, one could see that he was tiring and we
decided to say our goodbyes and I left. It was the best
day I had ever spent with him. My favourite email I have
ever received from him was received on the 12th of June
2015 and stated: “Dear Jens. Here are the proofs of my
review of your excellent book which should appear in
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
.—
Fig. 33. 2017 Herpetological Association of Africa’s Conference
in Bonamanzi, South Africa. From left to right: Werner
Conradie, Tyrone Ping, Prof. William Branch, Luke Verburet,
Dr. Michael Bates, Johan Marais, Prof. Graham Alexander,
Prof. Aaron Bauer, Jens Reissig, Coleen Tiedemann, Dr. Colin
Tilbury, and Dr. Victor Loehr (Photo: Andre Coetzer).
Herp Review this month. Hope you're happy with it and
all goes well. Best wishes. Bill”
Professor W.R. Branch, your passing has left a
massive hole in so many people’s lives and in African
Herpetology as a whole. Your knowledge and sense of
humour will be greatly missed by anyone who ever had
the privilege to know you and who’s life you may have
affected in some way or another. Africa has lost two
great herpetologists way too soon and in relatively quick
succession. Till we meet again!
Harold Braack
South Africa
Bill Branch first came into my life, I think, in 1974,
at an HAA conference held at Skukuza in the Kruger
National Park (KNP). It might have been the first such
get-together. At that time, I was doing the herpetology
survey of the KNP, so it was indeed fortuitous to meet
Bill Branch, as well as Don Broadley and Carl Gans.
In 1976, I was transferred to the Bontebok National
Park and so I started species surveys and checklists. I
wanted to know what it was that I was supposed to be
looking for, and so Bill and I started working together
through various National Parks and adjacent areas. But
it was not only herps. We looked at succulent plants and
birds as well.
What Bill gave me was the confidence to do the
surveys. In him, I had a partner with whom I could share
my passion for conservation and protection of all the
inhabitants of those areas. He was totally enthusiastic
and this rubbed off on us all. Above all, he was a good
friend.
I have many fond memories of Bill, but share only a
few here.
The pepper ticks at Addo National Park were a vast
irritation to Bill. We picked them up every time we
ventured on a collecting trip. He hated them. I wiped
them off with paraffin. But Bill had a different solution.
Amphib. Reptile Conserv.
“Oh no,” he said. “I go home. I get undressed completely
then lie down in the nude on the kitchen counter. My
family has to pick them off. “
Bill Duellman and Bill Branch stayed with us in the
Karoo for several days. To separate the two, we called
Duellman “Bill” and Branch “Billikins.” Bill B. was not
totally enamoured with the solution.
Bill and I did a night road survey in the Richtersveld.
After several hours we arrived at Paradyskloof. We lay
down flat on our backs for a while counting passing
satellites, then later scratching among the rocks where
we saw the largest Hadogenes that either of us had seen.
Then Bill went to the little pool to find a Strongylopus
springbokensis. Ka-splash, splash. Bill fell in the pond.
He sat huddled in the bakkie on the way home.
Spending a long, long time trying to catch a lizard in
Richetrsveld, Bill suddenly ran back to the bakkie. Out
he came with a revolver loaded with dust shot. “Ka-
boom!” he shot the thing—we had our specimen.
He had excellent repartee and a quick lucid mind.
How many of us remember his response during a frog
meeting at Stellenbosch? The chair said we should be
democratic in the course of the meeting. Bill’s immediate
response “Thank You, Mr. Mugabe.”
Bill also enjoyed fishing, especially for carp. We spent
some time along the banks of the Orange and Breede
Rivers doing just that. Didn’t catch much, but those were
relaxing times.
I best remember Bill as a man who was a dear friend.
To all of us, he revealed the treasure chest of our vast
herpetological wealth—and, more, he opened it up for us
to see and explore. He followed his passion with a radiant
glee which he passed on to us.
Bill, my friend, I salute you for being a friend, a guide,
and an explorer who found and revealed.
Atherton de Villiers
CapeNature, Western Cape, South Africa
I have good memories of Bill that date back to when his
career 1n herpetology started at Port Elizabeth Museum,
and have always admired his enthusiasm and vast
knowledge of reptiles and amphibians. It is well known
that one of his greatest achievements was his Field Guide
to the Snakes and other Reptiles of Southern Africa. This
landmark publication opened up the world of reptiles to
countless numbers of people, and it was a pleasure to
contribute information and images for one of the most
important herpetological publications in southern Africa.
I share with you all the huge loss of Bill to herpetology,
biodiversity conservation, and life in general.
Marius Burger
North-West University, South Africa
Try as I may, I just can’t seem to pinpoint the precise
memory of actually meeting Bill for the first time. ?'m
quite shocked by this realisation. I presume that it was
sometime during 1987 when I was a young (20 y/o)
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Conradie et al.
Fig. 34. Ozzy Osbourne meets Elvis Presley. My all-time
favourite photo of Bill and I (Photo: John Measey).
nature conservation student in Grahamstown, and I
vaguely remember something about visiting him at
his office at Port Elizabeth Museum (PEM). The only
definite lead that I have to go on is a specimen of Karoo
(ex-Namaqua) Plated Lizard (Gerrhosaurus typicus)
that I collected in November 1987 on the Karoo Nature
Reserve in Graaff-Reinet. At the time, this record
represented an eastern distribution range extension
of 211 km. Whoopee! I would have hurriedly taken
the specimen to Bill at PEM, with my tail wagging in
excitement. Yes, what a joy it always was to make some
sort of new herpetological discovery that even The Bill
Branch would find somewhat noteworthy. And so it came
to pass that my first ‘scientific publication’ was a short
note in the Journal of the Herpetological Association
of Africa (Burger 1988). The truth be known, Bill
actually wrote the damn thing. But this was my official
introduction to the Herpetological Association of Africa,
and it marks the approximate start of a very lekker 30-
year friendship with Bill.
An article published in Zootaxa on 24 October 2018
demonstrated that the African Slender-snouted Crocodile
(Mecistops cataphractus) is in fact comprised of two
superficially cryptic species, and thus M. leptorhynchus
from Central Africa was resurrected as a valid species
(Shirley et al. 2018). The first thought that crossed my
mind when I read this paper was “Fok, Bill didnt get
to see this!”, because Bill had died ten days earlier. Bill
would have loved the news that Mecistops is monotypic
no more, and perhaps (probably) he even knew that this
was in the pipeline. Fast-forward nine months to July
2019 (i.e., right now as I’m writing this), and I’m still
experiencing Where-TF-is-Bill moments on an almost
daily basis. Bill was my Google Herps. Whenever
I needed photos of far-flung African reptiles to be
identified, the oh-so-convenient Google Herps would
Amphib. Reptile Conserv.
Fig. 35. Bill emerging from swamp in Gabon (2002) after
checking funnel traps that he had set with the hope of catching
an African Parachanna (Photo: Marius Burger).
Ue
usually be my first check. When the complexities of
taxonomy would bewilder my brain, Bill had the knack
of explaining it in a way that I could sort of comprehend.
And so for me, it is not only very sad, but also utterly
inconvenient and totally kak that Bill died.
It always intrigued me that a Pom could arrive in
Africa with some sort of medical doctorate degree,
something to do with foetal rabbit liver metabolism and
primary liver cancer, only to end up perusing a career of
chasing reptiles and amphibians. Like, how the hell did
that happen?! Anyway, it’s a good thing that it turned out
the way it did. Well, so says I, because I have derived
much joy and intellectual enrichment from the times
hanging out with Bill. To South Africans, Bill was loved
and respected as our local herp guru. He was of course
also internationally renowned for his herpetological
contributions, and the momentum that he built up over
the decades will have him publishing papers for a long
while after he clocked out.
Fig. 36. Bill receiving medical attention during a biodiversity
survey of Loango National Park (2002). If I remember correctly,
it had something to do with removing ticks from a place where
the sun don’t shine (Photo: Carlton Ward Jr.).
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Tributes to William Roy Branch (1946-2018)
This may be somewhat of a narcissistic trait of mine,
but I like it that Bill liked me. I would often purposefully
say and do socially objectionable stuff in Bill’s presence,
for the reward of his approval and appreciation of
my crudeness. Now that I think about it, this kind of
behaviour was probably akin to a son showing off in
front of his father for attention and approval. In a book
that collated a collection of interviews on how to become
a herpetologist (Li Vigni 2013), Bill wrote the following:
“T also never miss a chance to be with Marius Burger,
just to re-emphasize how sane I am.” Whenever Bill
acknowledged me in a publication, I would smile, and
feel all warm and gushy inside for receiving his praises.
In the acknowledgments section of Tortoises, Terrapins
& Turtles of Africa (Branch 2008), Bill wrote: “A special
thanks to Marius Burger, whose tortoise photography is
Just too good.” Well, just imagine the grin on my face for
that bit of flattery. He then went on to say: “...ifhe could
only look after his camera lenses as well as his hair...”
in The Dangerous Snakes of Africa (Spawls and Branch
1995), and Bill included a thanks to a certain Marias (sic)
Birger (sic) for companionship and advice. If that was
indeed me that he was referring to, then I say ditto to that.
Whilst on a fieldtrip with Olivier Pauwels and Bill
Branch in Gabon, the three of us shared a shipping
container that was modified into a bedroom of sorts. I
retired to bed late one evening, with Olivier and Bill
giggling away like preteen girls. The reason for their
hysterics was that they had planted a condom half-filled
with Condensed Milk in my bed. How silly 1s that!
Anyway, I never noticed said condom in my bed and
managed to fall asleep in spite of the spurts and snorts
of laughter. The next day whilst checking our trap arrays
they told me of their really funny prank, all the while
grinning from ear to ear as they awaited my reaction.
Instead of shock and dismay, I replied with a calm
reminder that a cleaning team was making our beds each
morning and just imagine what their take would be on
discovering this soggy item in one of our beds. I watched
as their expressions gradually turned from smile to mild
alarm, as the two of them slowly processed and realised
the gravity of this scenario. Now it was my turn to laugh.
I’m not a spiritual kind of guy, and thus I won’t be
saying things like RIP. old friend or check you on
the other side. But ja, Bill was for sure a significant
component of my life. Iam very chuffed to have had him
as a friend.
Mike Raath
Director, Port Elizabeth Museum Complex (now
Bayworld), 1987-1995
I first met Bill Branch in the early 1980s, when I was
at Wits University as head of the Bernard Price Institute
for Palaeontological Research. I had been invited by
Prof. Brian Allanson of Rhodes University’s Zoology
Department to present a short course on the evolution
of the Class Reptilia at my much loved Alma Mater.
Amphib. Reptile Conserv.
At that early point in my career, I only knew of Bill
by reputation, and had never met him personally. I felt
flattered that he had taken the time and trouble to travel
from Port Elizabeth to Grahamstown to listen to my
ramblings. I little realised then that he and I would meet
up again in a different context several years later, when I
was fortunate enough to be appointed Director of the Port
Elizabeth Museum Complex, as it was then called before
it got its trendy current name of “Bayworld.’
Bill was a much-respected member of the research
staff of the Complex, having charge of one of the most
comprehensive and important herpetological collections
in the country, building on the solid legacy of its original
founder, the legendary F.W. FitzSimons, almost a century
before. He was one of the stars of our research team,
regularly producing work that was published in some
of the world’s top peer-reviewed scientific journals. But
in addition, he was a prolific writer of popular articles
and books aimed at the general reader that spread his
expert knowledge to a much wider general readership.
I remember one envious member of our research staff
calling him “the Naas Botha of our research team” in
terms of earning brownie-points for research output (only
those who know something about South African rugby in
the 1980s will understand that comment! ).
One of the things that defined Bill was his off-the-
wall unconventionality. I remember how audiences at
his various public presentations would shudder in shock,
horror, and jaw-dropping disbelief when he demonstrated
his go-to technique for distinguishing between identical
sibling species of toads—by licking them! And, by Jove,
it worked!
I respected Bill as a person and as a scientist. But to be
candid, I have to say that he and I did not get on that well
personally. He suffered neither fools nor administrators
gladly, so as his director I guess I failed on both counts!
But as a scientist committed to his discipline there was
no faulting him. He was single-mindedly devoted to his
collection and his research, often to be found in his lab
or office over weekends or public holidays when most
others on the staff were taking what they rightly regarded
as a well-earned rest.
One particular Saturday morning remains starkly and
darkly etched in my memory, when Bill received an urgent
call in his lab mid-morning from the Snake Park. One
of the Snake Handlers, Mr. Nimrod Mkalipi, had been
bitten by a Puff Adder at the end of the daily live snake
demonstration, and he was in dire distress. Bill dropped
everything and rushed to Nimrod’s side, administering
antivenom and applying appropriate emergency first
aid. Tragically, though, it was to no avail and Nimrod
succumbed on the scene despite Bill’s urgent, expert, and
devoted efforts. Medical opinion afterwards held that it
was anaphylactic shock that took Nimrod’s life, and that
nothing other than immediate on-site specialised medical
intervention would have had any chance of preventing
it. That event shocked us all. It is a dark memory that I
September 2019 | Volume 13 | Number 2 | e186
Conradie et al.
I si ee ee ee
Fig. 37. Bill walking off into the early morning light to
photograph some Welwitschias in south-western Angola in
2009 (Photo: Werner Conradie).
carry with me to this day, but I applaud Bill Branch for
his swift reaction and his valiant and urgent attempts to
save the life of a fellow staff member. We all had much
to learn from that tragedy.
Werner Conradie
Port Elizabeth Museum, South Africa
The first time I became aware of Bill was when I
attended my very first HAA conference at Bayworld in
2004, which he organised. I remember the occasion very
clearly, as the only options available at the icebreaker
were beer, and Coca-Cola. I was too shy to speak to him
then—he was the famous Bill Branch and I was, after
all, just a lowly student. I met Bill again at the 2006
HAA held at Potchefstoom, and this time I was on the
organising committee. At this event I recall fondly Bill’s
talk on ‘guts and gonads,’ which of course went well
over its allotted time. However, it wasn’t until I finished
university completely that we would have what would
turn out to be a bit of a prophetic chance encounter.
While on a December break, just before I would start a
new job as a Physical Science high school teacher, me
and my now wife walked into him while strolling around
the museum. I introduced myself to him, finally having
a moment in his direct eyesight after all this time, and
with a curt nod paired with a brief “nice to meet you,” he
disappeared through the door to his lab and office. Never
would I have guessed that less than six months after this,
I will be sitting in front of him for an interview for the
job of Assistant Herpetologist. I must have impressed
Bill one way or the other (couldn’t have been pure
desperation), as two days later I received a call that I got
the job. I finished my contract at the school as fast as I
could, and with great excitement walked straight into the
museum the very same day. Bill looked at me in utter
shock and sent me home, saying I should come back in
the New Year... I guess he wasn’t prepared for my quick
start!
For the first year at the museum I had to learn all
the ropes. Now this is a very steep uphill battle for
Amphib. Reptile Conserv.
Fig. 38. Bill holding a Meller's Chameleon (7rioceros melleri),
looking radiant despite a very tiring hike during the summit of
Mt. Mabu in 2009 (Photo: Werner Conradie).
an Afrikaans-speaking seun that knew his frogs, but
no reptiles. Up to that point in time, the only reptile
ever caught by me was a harmless Common Brown
Water Snake. The first challenge I faced was getting
into a conversation with Bill. Because of his British
heritage, he mumbled a lot and this made me struggle to
understand his pronunciation of scientific names. After
many “conversations,” I often went back to my office
and paged through his field guide to prepare for the next
engagement. Bill, however, never forced his reptilian
inclinations on me. Once, he walked into my office and
promptly asked me what I wanted to specialise in, to
which my response was tadpoles. He dryly remarked that
the only thing they are good for is fish bait. As it turns
out, I never did work on tadpoles that much...
I went into the field with Bill for the first time as part
of a multi-collaborative expedition to Angola in 2009.
Bill didn’t have to bring me along, he could have kept
all the new places and specimens to himself, but I will
ever be grateful as it was on that trip that I fully came
to understand and realise what my responsibilities as a
museum herpetologist include: New discoveries! I joined
Bill on two more consecutive trips to Mount Mabu,
Mozambique in 2009 and Lagoa Carumbo, Angola in
2011. It was at this stage that Bill assisted me with my
first-ever species description, and just as I was starting to
bask in the glow of his knowledge, he clearly thought he
had trained me enough and turned off the light. It seemed
I was on my own: Bill expected me to swim. It was up to
September 2019 | Volume 13 | Number 2 | e186
Tributes to William Roy Branch (1946-2018)
me to show him that I could. We wouldn’t go on another
field trip together again until 2015, again to Angola. By
this time, Bill had retired, and I was keeping the fort on my
own. During the trip, around the campfire one evening,
Bill told me that he can now rest in peace, knowing the
Port Elizabeth Museum herpetology collection is in good
hands. Thank you, Bill.
I worked with Bill for more than ten years, but I only
really started to get to truly know him and his family
when he was unfortunately diagnosed with motor neuron
disease. It was a devastating experience to see your
mentor and friend fade away in front of your eyes. Bill
was determined to follow his passion to the very end, and
his determination was amazing to behold. Bill has taught
me life lessons that I will cherish forever. He was truly a
one-of-a-kind man. He is and will be missed.
Martin J. Whiting
Department of Biological Sciences,
University, Sydney, Australia
I first met Bill in 1994, just as I was about to start my
Ph.D. working on flat lizards (Platysaurus). I was based
at the Transvaal Museum in Pretoria, and he arrived to
Slice up snakes as part of a project on the ecology of
African snakes with Rick Shine, Jonathan Webb, and
Peter Harlow. Shortly after meeting him, he told me about
the Augrabies flat lizard system, which ended up being
the subject of my Ph.D. and many happy field seasons.
I owed him a huge debt, without realising it at the time!
And as it turned out, our discussions about flat lizards led
to a collaboration that continued until his death.
Everyone that meets Bill is immediately struck by
how warm and caring he is. It’s hard to describe, but
he had a personality that immediately drew you in. And
I think that’s why he had such an impact on so many
people. He was particularly giving and helpful to young
aspiring herpetologists, and I very much appreciated his
friendship and advice as a young Ph.D. student fresh on
the herpetological scene in South Africa. A few years
into my Ph.D., he invited me on a field trip to a remote
area of northern Mozambique to survey the vertebrates
of the Moebase region, the site of a proposed titanium
mine (sadly). I really appreciated this gesture, because
he could have invited any number of far more qualified
people! His son Tom was also on the trip, to survey
birds. Little did I know that this would become such
a memorable trip, and that I would have experiences I
still talk about to this day. There is nothing like a field
trip to really get to know someone, and that trip forged a
lifelong friendship. With Bill, there was never a shortage
of stimulating conversation on a wide range of topics
beyond herpetology. His love for natural history was
Macquarie
Amphib. Reptile Conserv.
XXVviii
infectious. The only thing Bill spoke about with more
passion was his wife Donvé. While on that same field
trip to Mozambique, Bill set out to find a clay pot that
was representative of the region, to take back to Donveé.
I should mention that Donvé is an award winning potter,
so this was the perfect gift! Our fixer couldn’t quite
understand what a westerner would want with a clay pot,
but we examined quite a few, before buying one from
a surprised local villager. Actually, I also acquired one
which has survived multiple moves in South Africa and
a final move to Australia. (How could I not buy one after
hearing Bill wax on about Donveé and her pottery!)
Bill was larger than life and made a huge impact on
African herpetology. It’s hard to accept that he’s gone, but
he will never be forgotten. He will certainly be missed by
many. I am currently working on finishing a phylogeny
and revision of the Platysaurus with Scott Keogh
and Mitzy Pepper, a project that Bill and the late Don
Broadley were both involved in, and he will certainly be
in our thoughts as we put together the final touches.
Fig. 39. Bill and his son Tom while passing through a village
during our 1997 Mozambique trip (scanned from a slide). To
this day, that field trip ranks as one of my most memorable
(Photo: Martin Whiting).
egeerie BA ee io ee at ie
Fig. 40. Bill in action during our 1997 Mozambique trip
[scanned from slides] (Photo: Martin Whiting).
September 2019 | Volume 13 | Number 2 | e186
Literature Cited
Conradie et al.
Li Vigni F (Editor). 2013. A Life for Reptiles and Amphibians,
Volume 1. Chimaira, Frankfurt, Germany. 495 p.
Branch B. 2008. Tortoises, Terrapins & Turtles of Africa. | Shirley MH, Carr AN, Nestler JH, Vliet KA, Brochu
Struik Publishers, Cape Town, South Africa. 128 p. CA. 2018. Systematic revision of the living African
Burger M. 1988. Geographical distribution: Gerrhosaurus Slender-snouted Crocodiles (Mecistops Gray, 1844).
typicus. Journal of the Herpetological Association of Zootaxa 4504(2): 151-193.
Africa 35: 36.
Amphib. Reptile Conserv.
Spawls S, Branch B. 1995. The Dangerous Snakes of
Africa. Southern Book Publishers, Halfway House,
Johannesburg, South Africa. 192 p.
Werner Conradie holds a Masters in Environmental Science (M.Env.Sc.) and has 12 years
of experience with the southern African herpetofauna. His main research interests focus on
the taxonomy, conservation, and ecology of amphibians and reptiles. Werner has published
numerous principal and collaborative scientific papers, and has served on a number of
conservation and scientific panels, including the Southern African Reptile and Amphibian
Relisting Committees. Werner has undertaken research expeditions to various countries
including Angola, Botswana, Lesotho, Malawi, Mozambique, Namibia, South Africa, Zambia,
and Zimbabwe. He is currently the Curator of Herpetology at the Port Elizabeth Museum
(Bayworld), South Africa.
Michael L. Grieneisen spent much of his childhood searching for and observing herps in the
Appalachian Mountains of Pennsylvania, USA. He obtained a B.S. in Biology and Chemistry
from Shippensburg University in Pennsylvania, and a Ph.D. in Biology from University of
North Carolina, Chapel Hill, on a National Science Foundation graduate fellowship. Mike’s
Ph.D. and post-doc work (at University of Nevada, Reno) investigated the hormones that turn
caterpillars into butterflies. Over the past 12 years at University of California, Davis, Mike has
authored journal articles in fields as diverse as nanotechnology, climate change, biodiversity,
scientometrics, environmental science, and reduced-risk pest control practices in California.
Mike is a freelance editor, co-editor of Amphibian & Reptile Conservation, and he is compiling
metadata for the theses and dissertations on amphibians and reptiles produced worldwide.
The compilation currently includes over 54,000 theses, completed from 1803 to the present at
institutions in well over 100 countries, and is expected to be made available sometime in 2020.
He also has an extensive collection of world banknotes which feature herps in the design.
Craig L. Hassapakis is the Founder, Co-editor, and Publisher of the journal Amphibian &
Reptile Conservation (official journal website: amphibian-reptile-conservation.org), which
was founded in 1996, and a former editor of FrogLog (www.amphibians.org/froglog/). Craig
has been an instructor (first grade through college), non-profit and governmental volunteer at
Public Library of Science (PLoS), Co-group Facilitator, Genome Resources Working Group,
IUCN/SSC Amphibian Specialist Group (ASG), and is a member of the IUCN/SSC Amphibian
Specialist Group. His interests include biodiversity, evolution, systematics, phylogenetics,
taxonomy, conservation, and behavior of amphibians and reptiles. Craig is instrumental in
developing and establishing “Amphibia Bank: A genome resource cryobank and network for
amphibian species worldwide.” His professional memberships include: Society for the Study
of Amphibian and Reptiles (SSAR), Herpetologists’ League (HL), International Society for
Biological and Environmental Repositories (ISBER), and International Society for the History
and Bibliography of Herpetology (ISHBH).
XXix September 2019 | Volume 13 | Number 2 | e186
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 1-28 (e181).
A herpetological survey of western Zambia
Gabriela B. Bittencourt-Silva
Department of Life Sciences, Natural History Museum, London, SW7 5BD, UNITED KINGDOM
Abstract.—A list of 60 species of amphibians and reptiles found during a six-week survey in western Zambia
is presented. Two species of amphibians are newly reported for Zambia: Amietia chapini and an undescribed
species of Tomopterna, previously known to occur in the Democratic Republic of Congo and in Namibia,
respectively. Some of the material collected could not be confidently identified to species level because of
the taxonomic complexity and uncertainty of some groups (e.g., Phrynobatrachus, Ptychadena), even with
the use of DNA barcoding. This list is a small contribution to the growing knowledge of Zambian and African
herpetology.
Keywords. Amphibians, barcode, checklist, reptiles, Southern Africa, undescribed species
Citation: Bittencourt-Silva GB. 2019. Herpetological survey of western Zambia. Amphibian & Reptile Conservation 13(2) [Special Section]: 1-28 (e181).
Copyright: © 2019 Bittencourt-Silva GB. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Submitted: 2 September 2018; Accepted: 4 March 2019; Published: 6 August 2019
Introduction
Zambia is a landlocked southern African country
considered part of the Zambesiaca area, which also
includes Botswana, Malawi, Mozambique, parts of
Namibia (Caprivi), and Zimbabwe (Poynton and
Broadley 1991). Zambia is located on the main central
African plateau where elevations range from 1,200 m
to 1,500 m and the vegetation 1s dominated by miombo
woodland (Phiri 2005).
Very little has been published on the herpetofauna of
Zambia since the first then comprehensive reports from the
early 1900’s (see reviews in Haagner etal. 2000; Pietersen et
al. 2017). Poynton and Broadley’s compendium Amphibia
Zambesiaca (Poynton and Broadley 1985a,b, 1987, 1988,
1991) and Channing (2001) reported on the distribution of
Zambian amphibians, while Broadley (1971) presented an
initial treatise of the reptiles and amphibians of Zambia,
and Broadley et al. (2003) provided an updated atlas and
field guide to the snakes of Zambia. Similarly, Haagner et
al. (2000) and more recently Pietersen et al. (2017) have
made important contributions to Zambian herpetology.
Broadley (1991) presents a comprehensive list of
reptiles and amphibians from the Mwinilunga District,
northwestern Zambia, including records from museum
collections dating from 1957. However, except from the
extreme north-west (Hillwood Farm), the herpetofauna of
western Zambia remains very poorly studied, with only a
few regional checklists (e.g., Broadley 1991; Pietersen et
al. 2017).
Correspondence. g. bittencourt@nhm.ac.uk
Amphib. Reptile Conserv.
Currently, there are 189 species of reptiles recorded
for Zambia according to The Reptile Database (Uetz
et al. 2018) and 181 (two crocodile, 10 chelonian, 78
lizard, and 91 snake species) according to Pietersen
et al. (2017). The number of amphibian species varies
substantially according to different sources. Pietersen et
al. (2017) report 86 species of amphibians for Zambia,
while AmphibiaWeb (2018) reports 87 species, and
a search in the Amphibian Species of the World 6.0
database (ASW; Frost 2018) returns 104 species. This
disparity between databases is possibly due to the fact
that the ASW includes non-confirmed occurrences. An
example is the caecilian Boulengerula, which is expected
to occur in Zambia based on its known distribution but is
as yet unreported there.
Herein I present a checklist of species collected during
a six-week herpetological survey in western Zambia.
Materials and Methods
Study site and sampling
The survey was carried out in April and May 2014
encompassing protected as well as non-protected areas
of western Zambia (Fig. 1, Table 1). Figure 2 shows
the different vegetation types surveyed, comprising
miombo woodlands (dominated by Brachystegia spp.),
dry evergreen forests (dominated by Cryptosepalum sp.),
riverine forests (mushito) and grassy wetlands (dambo).
During the whole survey period there were only four
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
30
sinker mr. 10
Elevation (m)
M200 °° -15
Mi 430
|_| 660
890
1120
[) 1350
{| 1580
|_| 1810
|_| 2040
[__] 2270
[| 2500
Fig. 1. Map of Zambia showing sites surveyed for herpetofauna. The star indicates the capital (Lusaka).
days of rain and average temperatures were 30 °C during
the day and 15 °C at night. The main sampling methods
were acoustic and visual encounter surveys (diurnal
and nocturnal). Entomologists participating in the
expedition opportunistically collected some specimens
with the use of sweep nets and small pitfall traps (500
ml cups). All specimens collected were euthanized with
20% benzocaine (applied on the skin or in the mouth).
Samples of thigh muscles were taken and stored in
absolute ethanol before the specimens were fixed in 10%
formalin and transferred to 70% industrial methylated
spirit for long-term storage. All specimens are deposited
in the herpetological collection of the Natural History
Museum in London, United Kingdom (see Appendix 1).
Species identification
Identification keys for Amphibia (Channing 2001;
Poynton and Broadley 1985a) and Reptilia (Branch
1998; Broadley 1971: Broadley et al. 2003) were used to
Table 1. Localities in Zambia surveyed during this study. Protected areas are indicated by shaded green. NP: National Park; HQ:
Headquarters.
Locality District
Chavuma FR Chavuma
Hillwood Farm Ikelenge
Itezhi-Tezhi, Kafue NP Itezhi-Tezhi
Lukwakwa Kabompo
Livingstone, Maramba Lodge Livingstone
Mayukuyuku, Kafue NP Mumbwa
Nanzila Plains, Kafue NP Itezhi-Tezhi
Ngonye Falls Camp Shangombo
Nkwaji Mwinilunga
Sioma Ngwezi NP Shangombo
Sioma Ngwezi NP (HQ) Shangombo
Amphib. Reptile Conserv.
Longitude Latitude Elevation (m)
-13.07006 22.92880 1070
-11.26316 24.32782 1400
-15.77340 26.01151 1040
-12.66084 24.43697 1150
-17.89120 25.85821 900
-14.91533 26.06311 1010
-16.28138 25.91676 1030
-16.66139 23.57280 930
-11.56567 24.52605 1300
-16.89873 23.59847 1010
-16.66953 23.56743 1000
August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Fig. 2. Habitats surveyed in western Zambia. (A) Dambo and Cryptosepalum dry forest in Lukwakwa, (B) Dambo in Nanzila Plains,
(C) Miombo woodland in Nanzila Plains, (D) Margin of the Zambezi River at Ngonye Falls.
assist with the identification of specimens. Some species
identifications presented here are tentative because
some groups have complex and difficult taxonomies
(e.g., Hyperolius, Hemisus, Phrynobatrachus, and
Ptychadena). Most samples were barcoded to help
species identification (see details below). Despite its
known limitations (e.g., Deichmann et al. 2017; Hebert
and Gregory 2005; Meier et al. 2006), DNA barcoding
is generally, and sometimes very, helpful. The Basic
Local Alignment Search Tool (BLAST; Altschul et al.
1990) was used to search the GenBank repository and
identify the closest matches for each sample. As there are
not many 16S rRNA sequences of Zambian reptiles and
amphibians openly available for comparison, percentage
of sequence similarity presented here should be
interpreted with caution and while taking the possibility
of geographic isolation or isolation by distance into
account. Private databases were also used for sequence
comparisons (D. Portik and B. Zimkus). Snakes were
identified primarily using morphological characters.
Genetic analysis
Given the large amount of 16S rRNA sequence data
available in GenBank for African amphibians and
reptiles, this gene was selected for DNA barcoding. Total
genomic DNA was extracted using a Qiagen DNeasy
kit (Venlo, Netherlands) following the manufacturer’s
protocol for purification of total DNA from animal
tissues. A fragment (ca. 500 bp) of the 16S rRNA
Amphib. Reptile Conserv.
mitochondrial gene was amplified using the primers
16S H3062 (CCGGTTTGAACTCAGATCA) and 16SB
FROG (CGCCTGTTACCAAAAACAT) [modified from
Palumbi et al. 1991]. Polymerase chain reaction (PCR)
was performed using Illustra PuReTaq Ready-To-Go
PCR Beads (GE Healthcare Life Sciences) for 35 cycles
of 1 minute with annealing temperature at 51 °C. Single
strand sequencing reactions and electrophoresis were
carried out by the molecular lab team at the Natural
History Museum in London, United Kingdom. All
sequences generated are available in GenBank under
accession numbers MK464267—MK464483.
DNA sequences were trimmed in Genelous v.7
(Kearse et al. 2012) with a maximum of low-quality
bases of 20. Uncorrected pairwise distances (p-distances)
of the 16S sequences were calculated for some groups
in PAUP* (Swofford 2001). For Phrynobatrachus,
a maximum likelihood (ML) analysis with non-
parametric bootstrapping was carried out with RAxML
v.8.2 (Stamatakis 2014). The alignment was generated
in Geneious using the Auto algorithm of MAFFT v.7
(Katoh et al. 2002), inspected visually and poorly aligned
regions were eliminated using the GBlocks Server
v.091b (Castresana 2000). Evolutionary models were
evaluated using Automated Model Selection (using a
Neighbor Joining tree) in PAUP*. The best fitting model
(GTR + GAMMA) was selected according to the Akaike
Information Criteria (AIC). Tomopterna marmorata was
used for rooting.
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Results
A total of 40 species of amphibians (anurans) belonging
to nine families and 13 genera, and 20 species of reptiles
from nine families and 17 genera (14 lizards, five snakes,
one tortoise) were recorded during this survey (Appendix
1). Among the localities surveyed, Hillwood Farm had
the highest species diversity (n=23), followed by Nkwaji
(n=15). Different from all other areas surveyed, which
are characterized by a combination of miombo woodland,
dambo and/or dry forest, both localities mentioned above
have riverine or swamp forest, locally known as mushitos
(Fig. 2).
Species accounts
All collected specimens and their respective vouchers are
listed below. Voucher numbers in bold refer to specimens
identified solely based on morphology (i.e., no tissue
sample available).
Amphibia
Order Anura
Arthroleptidae
Arthroleptis stenodactylus Pfeffer, 1893
Shovel-footed Squeaker
Material. LUKWAKWA: BMNH 2018.5826, BMNH
2018.5827 (Fig. 3A), BMNH 2018.5828-29; NKWAJI:
BMNH 2018.5830. Comments: Found in leaf litter in
Cryptosepalum forest, in dambo and at edges of mushito.
Arthroleptis stenodactylus as currently understood is
widely distributed from Angola to Tanzania, and from
Kenya to South Africa. This taxon clearly represents a
species complex, possibly two ecologically distinct forms
(see comments in Pickersgill 2007). All specimens listed
above have white venters without any dark markings,
large inner metatarsal tubercles and a dark line on each
side running from the snout over the tympanum to the
shoulder. Sequence similarity with A. stenodactylus from
Malawi is 98% (GenBank accession numbers FJ51098—
99).
Arthroleptis xenochirus Boulenger, 1905
Plain Squeaker
Material. LUKWAKWA: BMNH 2018.5811 (Fig.
3B), BMNH 2018.5812—13; HILLWOOD FARM:
BMNH 2018.5814—20; NKWAJI: BMNH 2018.5821-—
25. Comments: Specimens were found in leaf litter in
Cryptosepalum and mushito. All specimens have a very
small tympanum and relatively large inner metatarsal
tubercle (when compared to A. xenodactyloides). The
closest match on GenBank (94%) is to A. xenodactyloides
from Malawi (FJ151103). There is no sequence of A.
xenochirus available for comparison.
Amphib. Reptile Conserv.
Bufonidae
Schismaderma carens (Smith, 1848)
Red Toad
Material. CHAVUMA FR: BMNH 2018.5729; ITEZHI-
TEZHI: BMNH 2018.5724—28 (Fig. 3C). Comments:
Specimens were found in miombo woodland. This
species 18 widely distributed in Zambia. The BLAST
result show 100% sequence similarity with S. carens
from South Africa (KF665176, AF220913).
Sclerophrys gutturalis (Power, 1927)
Guttural Toad
Material. CHAVUMA FR: BMNH_ 2018.5703;
LIVINGSTONE: BMNH 2018.5702; LUKWAKWA:
BMNH 2018.5705—06, BMNH 2018.5707,
MAYUKUYUKU: BMNH_ 2018.5701 (Fig. 3D);
NKWAJI: BMNH 2018.5704. Comments: This species
is found in miombo and Cryptosepalum forest. These
specimens lack the typical red infusions on their thighs,
although this could be due to preservation. Specimen
identification was confirmed using DNA barcoding
(100% sequence similarity with AF220876, from
Botswana).
Sclerophrys lemairii (Boulenger, 1901)
Yellow Swamp Toad
Material. HILLWOOD FARM: BMNH 2018.5723;
LUKWAKWA: BMNH_ 2018.5715—22 (Fig. 3E).
Comments: One male was found in a pond at night
and eight individuals were found in dambo near the
Cryptosepalum forest. About six males were calling
during the day and two couples were observed in
amplexus. The species exhibits dynamic sexual
dichromatism, where males undergo a temporary color
change (from dark green to bright yellow), depending
on the breeding period; females are reddish, especially
the parotid glands (Bittencourt-Silva 2014; Conradie and
Bills 2017).
Sclerophrys pusilla (Mertens, 1937)
Southern Flat-backed Toad
Material. ITEZHI-TEZHI: BMNH _ 2018.5709-10;
MAYUKUYUKU: BMNH_ 2018.5708 (Fig. 3F);
NKWAJI: BMNH — 2018.5711-12. Comments:
Specimens identification were confirmed using DNA
barcoding (100% sequence similarity) and non-
morphometric morphological characters following
Poynton et al. (2016). Specimens were found in miombo
woodland.
Hemisotidae
Hemisus cf. guineensis Cope, 1865
Guinea Snout-burrower
Material. HILLWOOD FARM: BMNH _ 2018.5801
(juvenile); LUKWAKWA: BMNH 2018.5800 (Fig. 3G);
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Bittencourt-Silva
“te a . »
Fig. 3. Amphibians of western Zambia. (A) Arthroleptis stenodactylus (BMNH 2018.5827), (B) Arthroleptis xenochirus (BMNH
2018.5811), (C) Schismaderma carens (BMNH 2018.5728), (D) Sclerophrys gutturalis (BMNH 2018.5701), (E) Sclerophrys
lemairii, (F) Sclerophrys pusilla (BMNH 2018.5708), (G) Hemisus cf. guineensis (BMNH 2018.5800), (H) Hemisus cf. guineensis
(BMNH 2018.5799), (1) Hemisus marmoratus (BMNH 2018.5713), (J) Hemisus marmoratus (BMNH 2018.5714), (KX) Hyperolius
dartevellei (BMNH 2018.5681), (L) Hyperolius major (BMNH 2018.5675), (M) Hyperolius marginatus (BMNH 2018.5667),
(N) Hyperolius nasicus (BMNH 2018.5666), (O) Hyperolius parallelus (BMNH 2018.5689), (P) Hyperolius parallelus (BMNH
2018.5697), (Q) Hyperolius quinquevittatus, (R) Kassina senegalensis.
Amphib. Reptile Conserv. August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
SIOMA NGWEZI NP: BMNH 2018.5799 (juvenile;
Fig. 3H). Comments: One juvenile (BMNH 2018.5801)
was found dead in a pitfall trap set for dung beetles near
mushito. One large individual (snout-vent length 42.2
mm) from Lukwakwa was found buried in sandy soil
under a log between Cryptosepalum forest and dambo.
The specimen from Sioma Ngwezi is a juvenile. The
BLAST search shows 95% sequence similarity with H.
guineensis from the Republic of the Congo (K Y080117—
19). According to Channing and Broadley (2002),
Hemisus barotseensis, which is endemic to western
Zambia, differs from H. guineesis and H. marmoratus
in body proportions. The presence of a bright yellow
vertebral stripe and small yellow spots on the back agree
with the description of H. barotseensis and it is possible
that these specimens are that species. If confirmed, this
would represent an extension both north and south from
its current known range.
Hemisus marmoratus (Peters, 1854)
Marbled Snout-burrower
Material. MAYUKUYUKU: BMNH 2018.5713 (Fig.
31); SIOMA NGWEZI NP: BMNH 2018.5714 (Fig. 3J).
Comments: Juvenile individuals found at night in sandy
soil in miombo woodland. Hemisus marmoratus is widely
distributed in sub-Saharan Africa, excluding rainforest,
and it mainly inhabits savannahs but can also be found
in gallery forests. The BLAST search shows the closest
match on GenBank (94%) is H. marmoratus (AY 531831).
Table 2 shows the p-distance for both species of Hemisus
presented here and highlights a limitation of the use of
this measure for species delimitation.
Hyperoliidae
Hyperolius dartevellei Laurent, 1943
Dartevelle's Reed Frog
Material. CHAVUMA FR: BMNH 2018.5681 (Fig.
3K); HILLWOOD FARM: BMNH _ 2018.5683-—84;
LUKWAKWA: BMNH — 2018.5682. Comments:
Specimens found in miombo woodland and edge of
mushito basking on vegetation during the day. According
to Channing et al. (2013) the snout profile of H.
dartevellei is truncated instead of shark-like or rounded,
but none of the specimens listed above have truncated
snouts. However, the BLAST results show 98-99%
sequence similarity with samples of H. dartevellei from
Ikelenge, north-western Zambia (JQ863650, JQ863653,
JQ863673, JQ863676—-78, JQ863704, JQ863708,
JQ863718, JQ863750, JQ863753—-54, JQ863756—-S9,
KY080197, KY080199).
Hyperolius kachalolae Schiotz, 1975
Kachalola Reed Frog
Material. HILLWOOD FARM: BMNH 2018.5676,
BMNH 2018.5677-80. Comments: Juvenile specimens
collected during the day on vegetation near a stream in
Amphib. Reptile Conserv.
mushito forest. In life, the overall coloration was green
with a faint canthal and dorsolateral line, consisting of
small spots. The green color faded after preservation,
although the line is still visible. This agrees with the
description provided by Schietz (1975). The sequenced
individual shows 98% similarity with H. kachalolae
from northern Zambia (D. Portik, pers. comm. ).
Hyperolius major Laurent, 1954
Material. HILLWOOD FARM: BMNH 2018.5675 (Fig.
3L). Comments: One male found on top of a leaf (1.5 m
from the ground) calling at night. Schietz (1999) reports
this as a savannah species from north-western Zambia
and eastern Democratic Republic of the Congo (DRC),
however, this specimen was found in a forest patch
(mushito). The closest matches from DNA barcoding
(97%) are H. kuligae and H. langi (D. Portik, pers.
comm. ). Schiotz (1999) states that these species found in
west and central Africa are very similar in morphology
and dorsal pattern, and may be conspecific. In contrast,
Kohler et al. (2005) treat H. kuligae as a western and H.
langi as an eastern Central African form. However, the
color pattern (especially the post orbital marking) differs
substantially from Laurent’s description of the type
material of H. /angi, whereas this specimen agrees with
the morphological description of H. major provided by
Schiotz (1999). There is no DNA sequence of H. major
available for comparison.
Hyperolius marginatus Peters, 1854
Margined Reed Frog
Material. LUKWAKWA: BMNH 2018.5667 (male;
Fig. 3M); NANZILA PLAINS BMNH 2018.5668,
BMNH 2018.5674 (juveniles). Comments: Specimens
found near ponds in miombo woodland. There is 100%
sequence similarity with H. marginatus from Zambia (D.
Portik, pers. comm. ).
Hyperolius nasicus Laurent, 1943
Pointed Long Reed Frog
Material. NANZILA PLAINS BMNH _ 2018.5666
(Fig. 3N). Comments: This single specimen was
collected during the day while resting on vegetation ca.
1 m above the ground in dambo. The specimen fits the
morphological description of the species provided by
Channing et al. (2013): when viewed in profile the snout
has a shark-like tip, and the first, third, and fifth toes have
one phalanx free (or nearly free) of webbing (see Fig. 4),
distinguishing it from all the other species. The closest
match on GenBank (98-99% sequence similarity) is
Hyperolius inyangae (JQ863674, JQ863683-—84), which
is only known from the Eastern Highlands of Zimbabwe
and Malawi (Channing et al. 2013). Although Channing
et al. (2013) provide accession numbers for the genetic
material of H. nasicus, no sequences could be found on
GenBank under this species name. This could be due
to sequence mislabelling and the accession numbers
August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Fig. 4. Details of head profile and webbing of Hyperolius
nasicus (BMNH 2018.5666). (A) Profile of head, (B) webbing
of right foot, and (C) schematic representation of webbing.
Scale bar represents 1 mm.
associated with H. invangae may actually be from H.
nasicus.
Hyperolius parallelus Giinther, 1858
Angolan Reed Frog
Material. HILLWOOD FARM: BMNH 2018.5687-88,
BMNH 2018.5689 (Fig. 30), BMNH 2018.5690-94,
BMNH 2018.5695; NKWAJI: BMNH_ 2018.5696,
BMNH 2018.5697 (Fig. 3P), BMNH 2018.5698—5700.
Comments: Specimens found near ponds in miombo
woodland. These specimens show a color variation
similar to the alborufus group (see Schiotz 1999).
Hyperolius parallelus is a taxonomically complex group
due to its considerable color polymorphism. According
to the BLAST search, the closest match (98% sequence
similarity with JQ513623, JQ513626, and JQ513625)
is H. angolensis from Angola (see Conradie et al. 2012;
Frost 2018).
Hyperolius quinquevittatus Bocage, 1866
Five-striped Reed Frog
Material. NKWAJI: BMNH 2018.5685—86 (Fig. 3Q).
Comments: Juveniles collected during the day while
resting on vegetation in mushito. BLAST results show
99% sequence similarity with H. quinquevittatus from
Ikelenge, north-western Zambia (GenBank accession
number JQ863752).
Kassina senegalensis (Dumeéril and Bibron, 1841)
Bubbling Kassina
Material. CHAVUMA FR: BMNH = 2018.5810;
HILLWOOD FARM: BMNH 2018.5802-03 (Fig. 3R);
NKWAJI: BMNH 2018.5804; SIOMA NGWEZI NP:
BMNH 2018.5805—09. Comments: Specimens found in
Table 2. Uncorrected pairwise distances (p-distances) for a fragment of the 16S rRNA gene for Hemisus spp. Distances between
conspecific populations are inside boxes.
Taxon ID 1 2 3 4 5
1 Hemisus marmoratus AY326070
2 Hemisus marmoratus DQ283430
3 Hemisus marmoratus AY531831
4 Hemisus marmoratus KY 176997
5 Hemisus marmoratus AY948749
6 Hemisus marmoratus KX492610
7 Hemisus marmoratus KM509138
8 Hemisus marmoratus KY 176998
9 Hemisus marmoratus BMNH 2018.5713
10 Hemisus marmoratus BMNH 2018.5714
11 Hemisus guineensis KY080117
12 Hemisus guineensis KY080118
13. Hemisus guineensis KY080119
14 Hemisus guineensis KY080120
15 Hemisus cf guineensis BMNH 2018.5799
16 Hemisus cf guineensis BMNH 2018.5800
17. -Hemisus cf guineensis BMNH 2018.5801
Amphib. Reptile Conserv.
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey
93
100
97
100
Namibia (GU457565)
100 | Lindi, Tanzania (KY177049)
Beira, Mozambique (DQ022361)
Tomopterna marmorata: Zambia (BMNH_2018.5792)
0.05
Ethiopia (FJ829292)
Ethiopia (FJ829296)
Ethiopia (FJ829295)
Ethiopia (FJ829297)
Uganda (FJ829298)
Ghana (FJ769126)
Ghana (FJ769127)
Céte d'Ivoire (GU457566)
Guinea (EU718726)
Sioma Ngwezi NP (BMNH_2018.5864)
Sioma Ngwezi NP (BMNH_2018.5865)
Ngonye Falls Camp (BMNH_2018.5836)
Ngonye Falls Camp (BMNH_2018.5855)
Mtunzini, South Africa (DQ019605)*
South Africa (DQ347303)
of western Zambia
Itezhi-Tezhi, Kafue NP (BMNH_2018.5848)
Itezhi-Tezhi, Kafue NP (BMNH_2018.5849)
Itezhi-Tezhi, Kafue NP (BMNH_2018.5850)
Nanzila Plains, Kafue NP (BMNH_2018.5851)
Nanzila Plains, Kafue NP (BMNH_2018.5852)
Mayukuyuku,
Mayukuyuku,
Mayukuyuku,
Mayukuyuku,
Mayukuyuku,
Mayukuyuku,
Mayukuyuku,
Maramba Lodge, Livingnstone (BMNH_2018.5853)
Maramba Lodge, Livingnstone (BMNH_2018.5854)
Lake Malawi Park, Malawi (FJ889462)
Kakamega Forest, Kenya (FJ889464)
Kakamega Forest, Kenya (FJ889463)
Tatanda Village, Tanzania (DQ283414)
Northern Territory, Rwanda (FJ829290)
Northern Territory, Rwanda (FJ829291)
Kigoma Region, Tanzania (FJ829299)
Tanzania (FJ829289)
lringa, Tanzania (FJ829293)
Kakamega Forest, Kenya (FJ889463)
Kakamega Forest, Kenya (FJ889464)
Kigoma Region, Tanzania (FJ829300)
Mangochi District, Malawi (FJ889462)
Niassa Game Reserve, Mozambique (FJ829303)
Niassa Game Reserve, Mozambique (FJ829301)
Niassa Game Reserve, Mozambique (FJ829302)
Morogoro Region, Tanzania (FJ829294)
Kafue NP (BMNH_2018.5837)
Kafue NP (BMNH_2018.5838)
Kafue NP (BMNH_2018.5839)
Kafue NP (BMNH_2018.5840)
Kafue NP (BMNH_2018.5841)
Kafue NP (BMNH_2018.5842)
Kafue NP (BMNH_2018.5843)
Haplotype
Group A**
Haplotype
Group B**
| Sp.2
| Phrynobatrachus natalensis
Nkwaji (BMNH_2018.5863)
Nkwaji (BMNH_2018.5858)
Nkwaji (BMNH_2018.5860)
Hillwood Farm (BMNH_2018.5866)
Nkwaji (BMNH_2018.5856)
Nkwaji (BMNH_2018.5859)
Nkwaji (BMNH_2018.5871)
Nkwaji (BMNH_2018.5872)
Nkwaji (BMNH_2018.5869)
Nkwaji (BMNH_2018.5868)
Hillwood Farm (BMNH_2018.5867)
Nkwaji (BMNH_2018.5870)
Sp.3
Fig. 5. Maximum likelihood phylogenetic tree inferred from nucleotide sequence data from mitochondrial 16S rRNA of
Phrynobatrachus natalensis. Numbers above branches are non-parametric bootstrap support values. Specimen vouchers or GenBank
accession numbers are shown in parentheses. Colored polygons highlight the clades comprising specimens from this study. (*)
Nearest sample from type locality of Phrynobatrachus natalensis; (**) Haplotype groups A and B in Zimkus and Schick (2010).
miombo woodland near temporary ponds. All sequences
closely match K. senegalensis (98%, GenBank accession
number AF215445).
Phrynobatrachidae (see Table 3 for inter- and intra-
specific p-distances; Fig. 5 shows maximum likelihood
tree for this group)
Phrynobatrachus cf. parvulus (Boulenger, 1905)
Small Puddle Frog
Material. HILLWOOD FARM: BMNH 2018.5873-78;
LUKWAKWA: BMNH 2018.5889 (Fig. 5A); NKWAJI:
BMNH 2018.5882 (juvenile), BMNH 2018.5879-80,
BMNH 2018.5883—88. Comments: All specimens were
found during the day in dambo. Males have a dark throat
(BMNH 2018.5882, BMNH 2018.5886—87). While the
specimens of P. mababiensis listed below have the venter
immaculate (creamy), these specimens have the venter
white with dark speckles. Additionally, these specimens
show a more well-defined band on the thigh (which
runs from knee to knee) and, in most specimens, a light
Amphib. Reptile Conserv.
line runs along the tibia-fibula and thigh (parallel to the
band) and joins a vertebral line above the vent (see Fig.
6A). According to Du Preez and Carruthers (2017), the
presence of the latter feature distinguishes P. parvulus
from P. mababiensis. However, this character is present
on both species and therefore cannot be used to separate
them (see Poynton and Broadley 1985a. Pietersen et al.
(2017) report P. parvulus for Ngonye Falls, approximately
25 km from Sioma Ngwesi NP, but unfortunately there
is no voucher specimen. Poynton and Broadley (1985a)
and Marques et al. (2018) provide discussions of the
literature on the identifications of P. mababiensis and
P. parvulus. The barcode is very inconclusive given
that the closest hits on GenBank (92-95%) include
samples of an unidentified species of Phrynobatrachus
from Gabon (KP247505), one from the Republic of the
Congo (KY080354), and P. keniensis (JX564885) and
P. scheffleri (FJ889479), both from Kenya. Poynton
and Broadley (1985a) suggest P. parvulus tends to be
associated more with upland and forest conditions than
August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Table 3. Uncorrected pairwise distances (p-distances) for the 16S rRNA gene for Phrynobatrachus spp. Distances between
conspecific populations are inside boxes. Dotted-line box indicates P. natalensis group.
1 Phrynobatrachus cf. parvulus BMNH 2018.5873
1
2
3
2 Phrynobatrachus cf. parvulus BMNH 2018.5874 0.01
3 Phrynobatrachus cf. parvulus BMNH 2018.5880 0.04 0.05 -
4 Phrynobatrachus mababiensis FJ889461 0.11 O12 0.12
5 Phrynobatrachus mababiensis BMNH 2018.5831 0.11 O11 0.12
6 Phrynobatrachus mababiensis BMNH 2018.5832 0.11 O11 0.12
7 Phrynobatrachus natalensis DQO019605 0.14 O15 0.14
8 Phrynobatrachus natalensis BMNH 2018.5855 0.14 O15 0.14
9 Phrynobatrachus sp. 1 BMNH 2018.5838 0.16 O17 0.17
10 Phrynobatrachus sp. 1 BMNH 2018.5839 0.16 O17 0.17
11 Phrynobatrachus sp. 3 BMNH 2018.5856 0.15 016 0.15
12 Phrynobatrachus sp. 3 BMNH 2018.5858 0.15 016 0.15
13 Phrynobatrachus sp. 2 BMNH 2018.5864 0.17 O17 0.18
14 Phrynobatrachus sp. 2 BMNH 2018.5865 0.17 O17 0.18
P. mababiensis. The localities where these specimens
were found are all upland and either inside or near forest,
therefore I refer them to P. cf. parvulus.
Phrynobatrachus mababiensis FitzSimons, 1932
Dwarf Puddle Frog
Material. MAYUKUYUKU: BMNH 2018.5831-32,
BMNH_ 2018.5881; NANZILA PLAINS: BMNH
2018.5833; SIOMA NGWEZI NP: BMNH 2018.5834—
35. Comments: All specimens are juveniles and were
found in dambo both during the day and at night.
According to Poynton and Broadley (1985a), it 1s not
easy to distinguish P. mababiensis from P. parvulus based
on external morphology, but they suggest that some
characters usually serve to separate them (1.e., labial and
subtympanic markings, and shape of tarsal tubercle).
The usual well-marked black and white barring on the
upper and lower jaws is rather faint on these specimens.
Zimkus and Schick (2010) suggest that there 1s cryptic
diversity within the P mababiensis group. The closest
match on GenBank is P. mababiensis (FJ889461; 99%
sequence similarity) from eastern Zambia, which belongs
to a population that is sister to the clade containing P.
ukingensis and P. ungujae (see Zimkus and Schick 2010).
Phrynobatrachus natalensis (Smith, 1849)
Snoring Puddle Frog
Material. NGONYE FALLS: BMNH _ 2018.5855.
Comments: The overall external morphology resembles
P. natalensis. The BLAST search shows 98% sequence
similarity to P. natalensis from Mtunzini, South Africa
(DQ347303), which is near Durban, the type locality of
P. natalensis (see Table 3 and Fig. 5).
Phrynobatrachus sp. |
Material. I[TEZHI-TEZHI:
50; LIVINGSTONE:
z)
BMNH
BMNH
2018.5848—
2018.5853—54;
Amphib. Reptile Conserv.
4 5 6 7 8 9 10 11 12 13 14
0.00
0.00 0.00
0.14 013 013
0.14 013 013
0.17 0.16 0.16}
017 0.16 0.16}
015 014 0.14} 0.09
0.05 0.08 0.08 7
0.05 0.08 0.08 0.00 |
MAYUKUYUKU: BMNH 2018.5837-38 (Fig. 6B),
BMNH 2018.5839-42 (Fig. 6C), BMNH 2018.5843,
BMNH 2018.5844—-47,; NANZILA PLAINS: BMNH
2018.5851-52. Comments: Specimens were found in
dambos. One juvenile was found ona beach of the Zambezi
River at Ngonye Falls. The closest match on GenBank
(99% sequence similarity) is P. natalensis DQ283414
from Tanzania (see Fig. 5). Zimkus and Schick (2010)
suggest that there are two species of P. natalensis in East
Africa, and these Zambian populations are more similar
to the central and southern populations corresponding to
Haplotype group B. It further corresponds to Zimkus et
al. (2010) P. natalensis Clade E. See further comments
in Discussion.
0.16 015 0153
0.17 0.16 0.16:
0.16 }
0.17 0.16
Phrynobatrachus sp. 2
Material. NGONYE FALLS: BMNH2018.5836; SIOMA
NGWEZI NP: BMNH 2018.5864—-65. Comments:
Morphologically, these specimens resemble P. natalensis
in terms of size, toe webbing and overall color pattern.
However, they present silver/white spots around the vent
(and ventral part of the thigh in BMNH 2018.5836). The
closest match on GenBank is P. natalensis from Tanzania
(95%; DQ283414). Although their range overlaps with
the Southern African geographic zone (populations A
and B) in Zimkus et al. (2010), these populations form
a southern Zambian clade, which is a sister group of the
eastern and western African clades (see Fig. 5). These
findings allude to further cryptic diversity in the group.
Phrynobatrachus sp. 3
Material. HILLWOOD FARM: BMNH 2018.5866—67
(Fig. 6D); NKWAJI: BMNH 2018.5856-57, BMNH
2018.5858-60, BMNH 2018.5861 (Fig. 6E), BMNH
2018.5862-63; BMNH 2018.5868-69 (Fig. 6F),
BMNH _ 2018.5870-72. Comments: All specimens
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
rs a
An «spi
ae ie i
: Nee
a
Fig. 6. onan fe western Zaria, (A) re of one (BMNH 2018.5889), (B) Phrynobatrachus natalensis
(BMNH 2018.5838), (C) Phrynobatrachus natalensis (BMNH 2018.5842), (D) Phrynobatrachus sp. 1 (BMNH 2018.5867),
(E) Phrynobatrachus sp. 1 (BMNH 2018.5861), (F) Phrynobatrachus sp. 1 (BMNH 2018.5869), (G) Xenopus poweri (BMNH
2018.5659), (H) Xenopus pygmaeus, (1) Ptychadena anchietae (BMNH 2018.5730), (J) Ptychadena cf. mossambica (BMNH
2018.5759), (IX) Ptychadena porosissima (BMNH 2018.5766), (L) Ptychadena porosissima (BMNH 2018.5769), (M) Ptychadena
porosissima (BMNH 2018.5770), (N) Ptychadena taenioscelis (BMNH 2018.5785), (O) Amietia chapini (BMNH 2018.5664), (P)
Pyxicephalus cf. adspersus (BMNH 2018.5791), (Q) Tomopterna sp. (BMNH 2018.5797), (R) Chiromantis xerampelina (BMNH
2018.5798).
Amphib. Reptile Conserv. 10 August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
are morphologically similar to P. natalensis, however
the BLAST search shows sequence similarity with
P. natalensis from South Africa (GenBank accession
number DQ347303) varying between 90-91% (see Fig.
5). These populations form a northern Zambian clade,
sister to southern, western, and eastern African clades.
Further investigation is needed to resolve the taxonomical
status of this group.
Pipidae
Xenopus poweri Hewitt, 1927
Power’s Clawed Frog
Material. HILLWOOD FARM: BMNH 2018.5654—58;
NKWAJI: BMNH 2018.5659 (Fig. 6G). Comments:
Specimens collected from a pond in miombo area. The
BLAST search shows 99% sequence similarity with X.
poweri from Ikelenge, north-western Zambia (GenBank
accession number KP345253). Furman et al. (2015)
removed this name from the synonymy of X. petersii and
reassigned the West African populations of X. /aevis to
this species.
Xenopus pygmaeus Loumont, 1986
Bouchia Clawed Frog
Material. HILLWOOD FARM: BMNH 2018.5651—52
(Fig. 6H), BMNH 2018.5653. Comments: Species
identification was based on their relatively small size and
the presence of a fourth claw. Specimens were found ina
small pool formed in a car track next to a riverine forest
(mushito). Recently, Wagner et al. (2013) presented
the first record of Xenopus pygmaeus for Zambia,
representing a significant range extension (about 1,300
km). This species belongs to the fraseri subgroup
and it was previously known to have its southernmost
distribution in the northern part of the DRC. The DNA
barcode corroborates the morphological identification
(99% sequence similarity with KF738291).
Ptychadenidae
Ptychadena anchietae (Bocage, 1868)
Anchieta's Ridged Frog
Material. ITEZHI-TEZHI: BMNH_ 2018.5735-36;
MAYUKUYUKU: BMNH 2018.5730-31 (Fig. 61),
BMNH = 2018.5732-34. Comments: Specimens
collected near water in miombo woodland. The closest
match (99%) is P. anchietae (AY517610) from Tanzania.
Ptychadena grandisonae Laurent, 1954
Grandison's Ridged Frog
Material. NK WAJI: BMNH 2018.5737-43. Comments:
Two juveniles and four males found in a pond in miombo.
This series fits the description for P. grandisonae in
Poynton and Broadley (1985a). The results of the
BLAST search show that the closest match (98%) is
Amphib. Reptile Conserv.
11
Ptychadena sp. (GenBank accession number KF 178892)
from Gabon.
Ptychadena cf. guibei
Material MAYUKUYUKU: BMNH_ § 2018.5764;
SIOMA NGWEZI NP: BMNH 2018.5765. Comments:
Specimens identified following the key in Poynton and
Broadley (1985a). Foot length of BMNH 2018.5765 is
slightly less than half the body length and thus, according
to the key, this specimen would be mossambica or cotti
(i.e. schillukorum). The BLAST result shows 96%
sequence similarity with P. porosissima (KY177058)
from Kenya. There is no sequence of P. guibei available
for comparison.
Ptychadena mapacha Channing, 1993
Mapach Ridged Frog
Material. MAYUKUYUKU: BMNH 2018.5772 (male).
Comments: Specimen collected near water in miombo
woodland. Following Poynton and Broadley (1985a),
this specimen should be assigned to P cotti, now a
synonym of P. schillukorum. However, this specimen
also fits the description of Ptychadena mapacha (not
included in the key), except for the white spots on the
posterior face of the tibia and a thin tibial line that are
present in the holotype (CAS 160535). The closest match
(89%) is P. porosissima (GenBank accession number
KY177058) from Kenya, and the sequence similarity
with P. schillukorum (KY177060) is 82%. There is
no sequence of P. mapacha available for comparison.
Although P. schillukorum is \isted in the AmphibiaWeb
database as occurring in Zambia, there is no reference
to the literature confirming this claim. Pietersen et al.
(2017) provided an unconfirmed record of P. mapacha for
Sioma Ngwesi. This record represents the northernmost
record of this species.
Ptychadena cf. mossambica (Peters, 1854)
Mozambique Ridged Frog
Material. ITEZHI-TEZHI: BMNH 2018.5753, BMNH
2018.5754-57; MAYUKUYUKU: BMNH 2018.5763;
SIOMA NGWEZI NP: BMNH 2018.5758—59 (Fig. 6J),
BMNH 2018.5760, BMNH 2018.5761. Comments:
The key in Poynton and Broadley (1985a) points to
P. mossambica, except for the skin folds that are not
continuous in these specimens. The authors note that
P. mossambica shows an east-west cline in size and
degree of webbing, where material from western
Zambia tends to be smaller (maximum SVL 28.9 mm)
than the series from Mozambique (maximum SVL 52.5
mm). The average SVL of this series is 34 mm. Most
specimens have a pair (sometimes two) of large dark
blotches on the scapular region. The closest match on
GenBank (93-94%) is Ptychadena cf. mossambica from
coastal Tanzania (KY177057). These specimens may
be referrable to PR mapacha Channing, 1993, for which
there is no available sequence data. Ptyvchadena mapacha
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
has recently been recorded in Ngonye Falls, south-west
Zambia by Pietersen et al. (2017), confirming Channing’s
(2001) prediction about its distribution.
Ptychadena nilotica (Seetzen, 1855)
Nile Grass Frog
Material. LIVINGSTONE: BMNH — 2018.5781;
NANZILA PLAINS: BMNH 2018.5773-76, BMNH
2018.5777—80. Comments: Specimens collected at night
near water in miombo woodland. Sequence similarity
with P. nilotica is 98% with KFO27211 and 99% with
KX836515 from the DRC. For further discussion about
this species see Dehling and Sinsch (2013) and Zimkus
et al. (2016).
Ptychadena obscura (Schmidt and Inger, 1959)
Material. HILLWOOD FARM: BMNH 2018.5766-67
(Fig. 6K), BMNH 2018.5768. Comments: These small
specimens (SVL ranges from 21.8 to 22.8 mm) fit the
description of P. obscura in Poynton and Broadley
(1985a). The specimens have a pair of dark marks on
the scapular region. The results of the BLAST search
show higher similarity (97-98%) to P. broadleyi
(GenBank accession number MH300600-02). This is an
unexpected finding considering that P. broadleyi is only
known to occur in the Mulanje Mountain and the Zomba
Plateau, in Malawi. These specimens from Zambia have
a light triangle on the snout distinguishing them from
P. broadleyi. Hence, the barcoding results should be
interpreted with caution.
Ptychadena oxyrhynchus (Smith, 1849)
Sharp-nosed Grass Frog
Material. HILLWOOD FARM: BMNH 2018.5783;
NANZILA PLAINS: BMNH 2018.5782. Comments:
Specimens collected near water in miombo woodland.
Sequence similarity with P oxyrhynchus from
Kwambonambi, South Africa (GenBank accession
number AF215403) is 99%.
Ptychadena porosissima (Steindachner, 1867)
Three-striped Grass Frog
Material. HILLWOOD FARM: BMNH 2018.5769 (Fig.
6L), BMNH 2018.5770 (Fig. 6M), BMNH 2018.5771.
Comments: This species, common in miombo woodland
near water bodies, was present in large numbers at
Hillwood Farm. Sequence similarity with P. porosissima
(GenBank accession number KF0O27212) from Rwanda
is 98%.
Ptychadena cf. taenioscelis Laurent, 1954
Stripe-legged Grass Frog
Material. HILLWOOD FARM: BMNH 2018.5784—-86
(Fig. 6N). Comments: Adult specimens found in pond.
These specimens have been identified using the key in
Poynton and Broadley (1985a). The closest match on
GenBank (95%) is P. taenioscelis from the Republic of the
Amphib. Reptile Conserv.
Congo (GenBank accession number KY080397). Perret
(1979) assigned records of taenioscelis from west and
central Africa to pumilio Boulenger. There seems to be
some confusion in the literature regarding the taxonomy
of these species, and a review of the group is needed.
Ptychadena upembae (Schmidt and Inger, 1959)
Upemba Ridged Frog
Material. HILLWOOD FARM: BMNH 2018.5750—
52 (last number is a juvenile); NKWAJI: BMNH
2018.574446 (juveniles), BMNH 2018.5747-49 (last
number is a juvenile); SIMA NGWEZI NP: BMNH
2018.5762. Comments: Following the key in Poynton
and Broadley (1985a), this series should be assigned to
Ptychadena upembae. The BLAST search shows that
the closest match (96%) is Ptychadena aff. porosissima
(GenBank accession number DQ525940) from Tanzania,
but it is important to note that there is no sequence of P.
upembae available for comparison.
Pyxicephalidae
Amietia chapini (Noble, 1924)
Chapin's River Frog
Material. HILLWOOD FARM: BMNH 2018.5660-61,
BMNH 2018.5662—63, BMNH 2018.5664 (Fig. 60),
BMNH 2018.5665. Comments: Specimens found near
streams in miombo woodland. The result of the BLAST
search shows that A. chapini is the closest match to
the specimens collected at Hillwood Farm (sequence
similarity with A. chapini of 96-98%). All specimens
have long legs (tibiofibula ~0.6 of snout-vent length),
as noted by Noble (1924). I note that the specimens
described as A. chapini by Channing et al. (2016) differ
from the specimens listed above in coloration — the
latter being darker. If these specimens are confirmed
to be A. chapini, this will be the first record of this
species for Zambia, but their presence in Zambia is
not surprising considering the proximity (ca. 380 km)
between the currently known populations from southern
DRC (Kundelungu National Park) and Hillwood Farm.
Pyxicephalus cf. adspersus Tschudi, 1838
Giant Bullfrog
Material. SIOMA NGWEZI NP: BMNH 2018.5787-
91 (Fig. 6P). Comments: All individuals collected are
juveniles. Hence, identification is tentative and based on
the geographic range of the species. The BLAST shows
95% sequence similarity to Pyxicephalus cf. adspersus
(DQ347304) and P. edulis (DQ022366).
Tomopterna marmorata (Peters, 1854)
Marbled Sand Frog
Material. LIVINGSTONE: BMNH — 2018.5792.
Comments: Juvenile found in a small pond at night.
Skin of dorsum and venter is smooth; venter is pale
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Bittencourt-Silva
Table 4. Uncorrected pairwise distances (p-distances) for the 16S rRNA gene for Zomopterna spp. Distances between conspecific
populations are inside boxes.
1 Tomopterna sp. "Shankara" AY255095 7
Tomopterna sp. BMNH 2018.5793
Tomopterna sp. BMNH 2018.5794
Tomopterna sp. BMNH 2018.5795
Tomopterna sp. BMNH 2018.5796
Tomopterna delalandii DQ283403 0.06 0.06
2
3
4
5
6 Tomopterna sp. BMNH 2018.5797
7
8 Tomopterna damarensis KX869909 0.07 0.06
9
Tomopterna cryptotis JX564898 0.06 0.06
10 Tomopterna marmorata BMNH 2018.5792 0.08 0.08
11. Yomopterna marmorata AY 255084 0.08 0.08
with a few dark markings under the throat; tympanum
indistinguishable; undivided sub-articular tubercle on
first finger. The closest match on GenBank (100%) is
Tomopterna marmorata (AY 255084) from Zambia.
Zomopterna sp.
Material. SIOMA NGWEZI NP: BMNH 2018.5793—
97 (Fig. 6Q). Comments: All individuals are juveniles
and were found at night close to a light-trap set to
collect beetles. The main morphological characters of
these specimens are: dorsal and ventral skin smooth;
immaculate venter; presence of a ridge below tympanum;
tympanum indistinguishable; and undivided sub-articular
tubercle on first finger. The closest match on GenBank
(99%) is Tomopterna sp. “Shankara” (AY255095), an
undescribed species from Namibia (Dawood et al. 2002).
Table 4 shows the p-distances among the closest matches
from GenBank.
Rhacophoridae
Chiromantis xerampelina Peters, 1854
African Grey Treefrog
Material. MAYUKUYUKU: BMNH 2018.5798 (Fig.
6R). Comments: This is a widespread species found in
miombo woodland. One adult individual found at night
on a tree near the campsite.
Reptilia
Order Squamata
Agamidae
Agama armata Peters, 1855
Northern Ground Agama
Material. NGONYE FALLS CAMP: BMNH 2018.2751
(Fig. 7A). Comments: One juvenile found basking
on a log by the Zambezi River. Sequence similarity is
Amphib. Reptile Conserv.
0.06 0.06 0.06 0.06
0.07 0.07 0.07 0.07 0.06 0.05
4 5 6 7 8 i) 10 11
0.05 0.05 0.05 0.05 -
0.02 -
0.06 0.06 0.06 0.06 0.03 0.02 -
0.07 0.07 0.07 0.07 0.06 0.05 0.06 -
00 [aon] -
98% with A. armata ZFMK 84990 (GenBank accession
number GU128447).
Chamaeleonidae
Chamaeleo dilepis Leach, 1819
Flap-necked Chameleon
Material. CHAVUMA FR: BMNH 2018.2755 (Fig.
7B), BMNH 2018.2756. Comments: Specimens were
found in miombo woodland on shrubs above | m. There
are currently seven subspecies in this group and based
on their distributions, these specimens represent C.
dilepis quilensis (Uetz et al. 2018). Sequence similarity
is 99% with Chamaeleo dilepis from Matema, Tanzania
(GenBank accession number AY927272).
Gekkonidae
Hemidactylus mabouia (Moreau de Jonnes, 1818)
Common Tropical House Gecko
Material. I[TEZHI-TEZHI: BMNH 2018.2742, BMNH
2018.2740; NANZILA PLAINS: BMNH 2018.2741.
Comments: Common species found in a variety of
habitats, including heavily degraded ones, though not
found in forests. The closest matches from GenBank are
Hemidactylus mercatorius (AY 863034) and H. mabouia
(AY 863038), both showing 94% sequence similarity.
Lygodactylus chobiensis Fitzsimons, 1932
Chobe Dwarf Gecko
Material. ITEZHI-TEZHI: BMNH 2018.2743 (female;
Fig. 7C), BMNH 2018.2744 (male) Comments:
Specimens found on tree-trunks in miombo. Identification
follows the key provided by Broadley (1971). The
rostral is excluded from the nostril and the male has
dark forward-directed chevron marks on the throat. The
female is yellow and white underneath (Fig. 7D). The
closest match from GenBank (95% sequence similarity)
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Fig. 7. Reptiles of western Zambia. (A) Agama armata (BMNH 2018.2751), (B) Chamaeleo dilepis (BMNH 2018.2755), (C}H(D)
Lygodactylus chobiensis (BMNH 2018.2743), (E) Pachydactylus punctatus, (F) Ichnotropis capensis (BMNH 2018.2750), (G)
Meroles squamulosus (BMNH 2018.2753), (H) Trachylepis cf. albopunctata (BMNH 2018.2765), (I) Trachylepis varia (BMNH
2018.2769), (J) Zyphlacontias rohani (BMNH 2018.2761), (IK) Crotaphopeltis hotamboeia (BMNH 2018.2776), (L) Philothamnus
hoplogaster (BMNH 2018.2775), (M) Rhamnophis aethiopissa ituriensis (BMNH 2018.2772), (N) Thelotornis kirtlandii (BMNH
2018.2760), (O) Atractaspis congica (BMNH 2018.2274), (P)-(R) Kinixys spekii.
Amphib. Reptile Conserv. 14 August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
is Lygodactylus chobiensis from Zimbabwe (GenBank
accession number GU593456).
Lygodactylus angolensis Bocage, 1896
Angola Dwarf Gecko
Material. NKWAJI: BMNH 2018.2767 (male), BMNH
2018.2766 (female). Comments: Specimens were
identified following the key provided by Broadley
(1971). In both specimens, the mental has a pair of lateral
clefts, resulting from fusion with a large postmental. The
male has nine preanal pores, which distinguish it from
L. bradfieldi. The closest match from GenBank (90%
sequence similarity) is Lygodactylus sp. from East Africa
(GenBank accession numbers GU593448-50).
Pachydactylus punctatus Peters, 1854
Speckled Thick-toed Gecko
Material. I[TEZHI-TEZHI: BMNH 2018.2757, BMNH
2018.2758 (Fig. 7E), BMNH 2018.2759. Comments:
Specimens found at night in dry leaf litter in miombo
woodland. All specimens have the dorsum covered
with sub-uniform granules. The closest matches from
GenBank (93% sequence similarity) are Pachydactylus
punctatus (AF449120) and P. scherzi (AY123379). As
the latter is only known from Namibia (Bauer and Branch
1995), I assign these specimens to P. punctatus.
Gerrhosauridae
Gerrhosaurus bulsi Laurent, 1954
Laurent’s Plated Lizard
Material. HILLWOOD FARM: BMNH 2018.2754.
Comments: One juvenile collected by the farm scouts in
dry miombo. The BLAST search shows the closest match
(98%) as Gerrhosaurus bulsi from Angola (KF717381).
Broadley (1971, 1991) referred the population of
Gerrhosaurus from Ikelenge (north-western Zambia) to
multilineatus but this was later contested by Haagner et
al. (2000). Bates et al. (2013) consider G. bulsi a valid
species and discuss the taxonomic problems regarding G.
multilineatus.
Lacertidae
Ichnotropis capensis (Smith, 1838)
Cape Rough-scaled Lizard
Material. CHAVUMA FR: BMNH = 2018.2746;
LUKWAKWA: BMNH 2018.2749, BMNH 2018.2747;
NANZILA PLAINS: BMNH_ 2018.2750, BMNH
2018.2748 (Fig. 7F); SIOMA NGWEZI NP: BMNH
2018.2745. Comments: All specimens are juveniles and
were found in miombo woodland. Sequence similarity
is 99% with [. capensis from Katima Mulilo, Namibia
(GenBank accession number JX962898).
Meroles squamulosus (Peters, 1854)
Savanna Lizard
Amphib. Reptile Conserv.
Material. NANZILA PLAINS: BMNH _ 2018.2753
(Fig. 7G); SIOMA NGWEZI NP: BMNH 2018.2752.
Comments: Two adult males found in miombo.
Sequence similarity 1s 96% with Meroles (Ichnotropis)
squamulosus from Laela, Tanzania (GenBank accession
number JX962897).
Scincidae
Panaspis cf. wahlbergi (Smith, 1849)
Snake-eyed Skink
Material. CHAVUMA FR: BMNH 2018.2738, BMNH
2018.2739. Comments: Specimens found during the day
in leaf litter. The closest match from GenBank (98%) is
Panaspis sp. (KU236726), from Katanga, DRC. Medina
et al. (2016) provide a molecular phylogeny of this genus,
which suggests that there is cryptic diversity within P.
wahlbergi.
Trachylepis cf. albopunctata (Bocage, 1867)
Angolan Variable Skink
Material. ITEZHI-TEZHI: BMNH — 2018.2762;
MAYUKUYUKU: BMNH_ 2018.2765 (Fig. 7H),
BMNH_ 2018.2763. Comments: Specimens found
during the day. The BLAST search shows 99-100%
sequence similarity with sequences from 7! varia clade B
(accession numbers MG605651—59), which was recently
assigned to Trachylepis cf. albopunctata by Marques et
al. (2018).
Trachylepis damarana (Peters, 1870)
Damara Skink
Material. SIOMA NGWEZI NP (HQ): BMNH
2018.2764. Comments: Morphologically similar to 7.
varia group. However, both its distribution and sequence
similarity (99%) match T. damarana (see Weinell and
Bauer 2018).
Trachylepis wahlbergii (Peters, 1869)
Wahlberg’s Striped Skink
Material. ITEZHI-TEZHI: BMNH 2018.2769 (Fig.
71); LUKWAKWA: BMNH = 2018.2768, BMNH
2018.2770; NK WAJI: BMNH 2018.2771. Comments:
Specimens found during the day on rocks (Itezhi-Tezhi),
dambo (Lukwakwa), and inside a tree trunk at Nkwaji.
According to Broadley (2000) these specimens fall in
the distribution range of 7. wahlbergii. The most similar
sequence from GenBank is 7’ wahlbergii from Zambia
(99%, accession number DQ234810).
Typhlacontias rohani Angel, 1923
Rohan's Blind Dart Skink
Material. SIOMA NGWEZI NP (HQ): BMNH
2018.2761 (Fig. 7J). Comments: One specimen was
found buried in sand and collected by Errol Pietersen. The
closest match on GenBank (90%) is 7. punctatissimus
(DQ316889). There is no sequence of 7. rohani available
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Herpetological survey of western Zambia
Fig. 8. Drawings of Rhamnophis aethiopissa ituriensis (BMNH
2018.2772). Head and anterior of body in dorsal, left lateral,
and ventral views. Scale bar 10 mm. Drawings by Ed Wade.
for comparison.
Colubridae
Crotaphopeltis hotamboeia (Laurenti, 1768)
White-lipped Herald Snake
Material. ITEZHI-TEZHI: BMNH 2018.2776 (Fig.
7K); HILLWOOD FARM: BMNH 2018.2773; SIOMA
NGWEZI NP: BMNH 2018.2777. Comments: All
individuals collected are juveniles and were found at
night in miombo woodland near rocks. The most similar
sequence on GenBank is C. hotamboeia from Malawi
(99%, accession number AY611816).
Philothamnus hoplogaster (Gunther, 1863)
Green Water Snake
Material. NANZILA PLAINS: BMNH 2018.2775 (Fig.
7L). Comments: Specimen found while eating tadpoles
and juveniles of Kassina sp. in a temporary pond during
the day. This species is similar to other Philothamnus
but usually smaller (Marais 2004). The closest match
on GenBank (99%) is P. hoplogaster from Mozambique
(accession number FJ913484).
Rhamnophis aethiopissa ituriensis (Schmidt 1923)
Large-eyed Green Tree Snake
Material. HILLWOOD FARM: BMNH 2018.2772 (Fig.
7M; Fig. 8). Comments: Specimen found in leaf litter of
riverine forest during the day. Broadley (1991) provided
the first record of this species for Zambia. Based on
distribution, this form represents the subspecies R. a.
ituriensis from Niapu in the DRC (see Eimermacher
2012).
Amphib. Reptile Conserv.
Thelotornis kirtlandii (Hallowell, 1844)
Forest Vine Snake
Material. HILLWOOD FARM: BMNH 2018.2760
(Fig. 7N). Comments: One juvenile was found at night
resting on green vegetation in riverine forest (mushito).
Species was identified using the key in Broadley (2001)
and the following characters were observed: top of
the head, including temporal region, is uniform green;
rostral and nasals are strongly recurved onto top of snout;
supralabials are white with small green spots.
Lamprophiidae
Atractaspis congica Peters, 1877
Congo Stiletto Snake
Material. HILLWOOD FARM: BMNH 2018.2274
(Fig. 70). Comments: One relatively large specimen
found in moist leaf litter inside a patch of mushito at
night. Broadley and Blaylock (2013): 232 expanded the
description of A. bibronii to accommodate the condition
of 19 midbody scales of A. congica (19-21 scales at
midbody). This specimen exhibits erratic counts of
19+17, the latter count predominating after the 84"
ventral.
Order Testudines
Testudinidae
Kinixys spekii Gray, 1863
Speke’s Hinge-back Tortoise
Comments: One specimen (Figs. 5P—R) was found in
mushito at Nkwaji. The carapace was hinged between the
7" and 8" marginals. The specimen was photographed
and released.
Discussion
This is a non-comprehensive list of the herpetofauna of
western Zambia. The survey was conducted shortly after
the general breeding season for amphibians and reptiles in
this part of the world, and consequently most specimens
collected are juveniles. For the same reason, most species
were not active, which made the search for them more
challenging. However, some species of amphibians were
active during the survey. Phrynobatrachus were heard
calling during the day and at night, and at least ten males
of Sclerophrys lemairii were calling during the day in
Lukwakwa (see Bittencourt-Silva 2014). The presence of
juveniles of /chnotropis capensis and adults of Meroles
squamulosus in sympatry is explained by their staggered
life cycles (see Broadley 1967, 1979).
DNA barcoding is an important tool for identifying
candidate species. However, there are a number of
caveats. For instance, for amphibians, Vences et al.
(2005a) propose a tentative 16S rRNA threshold at
5% for interspecific sequence divergence but also
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Bittencourt-Silva
highlight the broad overlap of intra- and interspecific
divergence values (see Vences et al. 2005b, p. 1,865)
that complicates the establishment of threshold values.
Using DNA barcoding alone can potentially lead to
simplistic diagnoses of putative species. Another issue
with DNA barcoding relates to the taxonomic accuracy
of public DNA databases (e.g., GenBank, BOLD,
EMBL). Misidentified sequences are not uncommon
(Bridge et al. 2003; Vilgalys 2003), which reinforces
the importance of vouchering all sequences deposited.
Table 2 shows that the intra-specific p-distances within
H. marmoratus are considerably large in some cases.
This could be partly due to geographic distances, given
that the specimens are from Ghana, Guinea-Bissau,
Kenya, and Tanzania. A taxonomic review of this group
is clearly necessary. Nonetheless, genetic data may be
crucial in cases where species are genetically different
but morphologically largely conserved. An example is
the mongrel frogs from Mozambique and Malawi, which
have ca. 5% interspecific divergences but are in general
phenotypically indistinguishable (Conradie et al. 2018).
Some of the taxa reported here could not be assigned
to currently recognized species based on DNA barcoding
and/or external morphology. For instance, based on
p-distances, some of the Phrynobatrachus specimens
represent putative new species (Table 3). Zimkus and
Schick (2010) suggest that there are at least two species
currently identified as Phrynobatrachus natalensis in
East Africa, and another two clades are reported from
western and southern Africa (Zimkus et al. 2010). The
phylogeny presented here indicates that there may be
more species of this group in western Zambia (see Fig.
5). Species identified here as P. cf. parvulus may be a
new species. These results corroborate the conclusions
of Zimkus and Schick (2010) and Zimkus et al. (2010)
that a taxonomic review of the genus Phrynobatrachus
is needed. Similarly, the Zomopterna population found in
Sioma Ngwezi NP could represent an undescribed species
(Table 4) previously reported from Namibia (see Dawood
et al. 2002). These taxa deserve further investigations
by specialists. It is often the case that original species
descriptions lack diagnostic details, including illustration
of characters, and/or type material may be lost or in poor
condition, all of which can contribute to inconclusive or
even incorrect species identification. Additional datasets
(e.g., bioacoustics, ecology) often provide important
information and can solve some of these taxonomic
conundrums.
The genus Ptychadena currently comprises 56
species, some (possibly many) representing species
complexes (e.g., Zimkus et al. 2016). Nineteen species
have been reported in Zambia (see genus account in
Frost 2018), eleven of which were recorded during this
survey. The lack of an updated key to the Ptychadena
of Zambia makes the species identification process
challenging. Similarly, barcoding is not helpful when
there are no reference sequences available. A search of
Amphib. Reptile Conserv.
GenBank for 16S sequences of Ptychadena shows that
41% of currently recognized species are not represented,
and 22% of the sequences available are either pending
confirmation or identified only to genus. The taxonomy
of this group is clearly in need of attention.
Except for a few areas—on the extreme north-west of
the country and along the Zambezi river—most of Zambia
remains poorly studied. Recently, Channing and Willems
(2018) described a new species of Ptychadena from the
northern part of the country, and a new cryptic species of
Polemon (Squamata: Lamprophiidae) described from the
DRC and Uganda is likely to occur in Zambia (Portillo
et al. 2019). The list of species provided here adds new
points to the map of the Zambian herpetofauna.
The herpetofauna of Zambia is mostly contained
in the Zambezian biogeographical core, with only the
south-western region forming part of the South African
core (sensu Linder et al. 2012). Not surprisingly, many
species found during this survey also occur in the DRC
(e.g., Channing et al. 2016), Angola (Conradie et al. 2016)
and Namibia (Dawood et al. 2002), including Amietia
chapini, recorded here for the first time from Zambia.
Four species of amphibians that Pietersen et al. (2017)
expected to occur near Ngonye Falls are now confirmed
to occur at Sioma Ngwezi NP (Kassina senegalensis,
Phrynobatrachus mababiensis, Ptychadena porosissima,
and Pyxicephalus adspersus). The still very incomplete
knowledge of the Zambian herpetofauna remains the
main obstacle to our understanding of its biogeography
and the conservation statuses of its constituent species.
Acknowledgements.—| thank the entomologists Hitoshi
Takano, Lucia Chmurova, and Lydia Smith for support in
the field. I am grateful to Errol Pietersen for assisting with
logistics and collection of specimens at Ngonye Falls,
and to Darren Pietersen for helping with identification of
some reptiles and providing valuable comments on the
manuscript. The expedition to Zambia would not have
been possible without the support of Richard Smith, to
whom I am extremely grateful. I thank Werner Conradie
and Mark Wilkinson for their valuable comments on the
manuscript. Ed Wade kindly provided the scale counting
of Atractaspis congica and the drawings of Rhamnophis
aethiopissa ituriensis. | thank Simon P. Loader for his
invaluable support. I appreciate the help of Dan Portik
and Breda Zimkus with identification of Hyperolius and
Phrynobatrachus, respectively. Permits to collect and
export specimens were issued by the Department of
Veterinary Services, Ministry of Livestock and Fisheries
Development (ICS#08417).
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Gabriela Bittencourt is a Brazilian evolutionary biologist with research experience in natural
history, evolution, ecology, and biogeography, and a particular focus on amphibians. Gabriela
has more than 15 years of herpetological laboratory and fieldwork experience in the Neo-
tropics, Africa, and Asia. Her research has focused on understanding phylogenetic relation-
ships and biotic distribution patterns of amphibians. Gabriela is currently a Research Assistant
in the Herpetology Group at the Natural History Museum, London, United Kingdom.
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Bittencourt-Silva
Appendix 1. List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession numbers, and
locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species
AMPHIBIA: ANURA
ARTHROLEPTIDAE
Arthroleptis stenodactylus
Arthroleptis stenodactylus
Arthroleptis stenodactylus
Arthroleptis stenodactylus
Arthroleptis stenodactylus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
Arthroleptis xenochirus
BUFONIDAE
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys gutturalis
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys lemairii
Sclerophrys pusilla
Sclerophrys pusilla
Sclerophrys pusilla
Sclerophrys pusilla
Voucher ID
BMNH 2018.5826
BMNH 2018.5827
BMNH 2018.5828
BMNH 2018.5829
BMNH 2018.5830
BMNH 2018.5814
BMNH 2018.5815
BMNH 2018.5816
BMNH 2018.5817
BMNH 2018.5818
BMNH 2018.5819
BMNH 2018.5820
BMNH 2018.5811
BMNH 2018.5812
BMNH 2018.5813
BMNH 2018.5821
BMNH 2018.5822
BMNH 2018.5823
BMNH 2018.5824
BMNH 2018.5825
BMNH 2018.5703
BMNH 2018.5705
BMNH 2018.5706
BMNH 2018.5707
BMNH 2018.5702
BMNH 2018.5701
BMNH 2018.5704
BMNH 2018.5723
BMNH 2018.5715
BMNH 2018.5716
BMNH 2018.5717
BMNH 2018.5718
BMNH 2018.5719
BMNH 2018.5720
BMNH 2018.5721
BMNH 2018.5722
BMNH 2018.5709
BMNH 2018.5710
BMNH 2018.5708
BMNH 2018.5711
Amphib. Reptile Conserv.
Field ID GenBank Locality Latitude
SL2109 MK464479 ~~ Lukwakwa -12.66084
SL2121 | MK464478 ~~ Lukwakwa -12.66084
SL2123, MK464477_ ~— Lukwakwa -12.66084
SL2128 = MK464476 ~~ Lukwakwa -12.66084
SL2221 MK464475 — Nkwaji -11.57728
SL2145 =MK464471 — Hillwood Farm -11.26316
SL2146 =MK464470 — Hillwood Farm -11.26316
SL2147, MK464469 — Hillwood Farm -11.26316
SL2148 = MK464468 — Hillwood Farm -11.26316
SL2152. MK464467 — Hillwood Farm -11.26690
SL2153. MK464466 — Hillwood Farm -11.26690
SL 2246 MK464465 — Hillwood Farm -11.26690
SL2122 MK464474 ~~ Lukwakwa -12.66084
SL2124 MK464473 ~~ Lukwakwa -12.66084
SL2125 MK464472 ~~ Lukwakwa -12.66084
SL 2200 MK464464 Nkwaji -11.60592
SL 2201 MK464463 = Nkwaji -11.60592
SL 2202 MK464462 = Nkwaji -11.60592
SL 2203. MK464461 Nkwaji -11.60592
SL2204 MK464460 = Nkwaji -11.60592
SL2102 Chavuma FR -13.07006
SL2108 = MK464294 ~~ Lukwakwa -12.66084
SL2107 MK464293 ~Lukwakwa -12.74275
SL 2111 Lukwakwa -12.66084
SL 2069 MK464296 Maramba Lodge, Livingstone -17.89120
SL2025 MK464297 = Mayukuyuku, Kafue NP -14.91533
SL2190 MK464295 Nkwaji -11.60592
SL 2245 Hillwood Farm -11.26690
SL 2112 Lukwakwa -12.66084
SL2113 Lukwakwa -12.66084
SL 2114 Lukwakwa -12.66084
SL 2115 Lukwakwa -12.66084
SL 2116 Lukwakwa -12.66084
SL 2117 Lukwakwa -12.66084
SL 2118 Lukwakwa -12.66084
SL 2119 Lukwakwa -12.66084
SL 2047. MK464291 _ Itezhi-Tezhi, Kafue NP -15.77340
SL 2053. MK464290 _ Itezhi-Tezhi, Kafue NP -15.77340
SL2012 MK464292. Mayukuyuku, Kafue NP -14.91533
SL2189 MK464289 = Nkwaji -11.60592
21
Longitude
24.43697
24.43697
24.43697
24.43697
24.53960
24.32782
24.32782
24.32782
24.32782
24.31666
24.31666
24.31666
24.43697
24.43697
24.43697
24.55448
24.55448
24.55448
24.55448
24.55448
22.92880
24.43697
24.28436
24.43697
25.85821
26.06311
24.55448
24.31666
24.43697
24.43697
24.43697
24.43697
24.43697
24.43697
24.43697
24.43697
26.01151
26.01151
26.06311
24.55448
Altitude
1063
1063
1063
1063
1291
1356
1356
1356
1356
1308
1308
1308
1063
1063
1063
1244
1244
1244
1244
1244
1073
1063
1101
1063
900
1012
1244
1308
1063
1063
1063
1063
1063
1063
1063
1063
1036
1036
1012
1244
August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
Sclerophrys pusilla BMNH 2018.5712 SL2191 MK464288 = Nkwaji -11.60592 24.55448 1244
Schismaderma carens BMNH 2018.5729 SL2105 MK464298 Chavuma FR -13.07006 22.92880 1073
Schismaderma carens BMNH 2018.5724 SL2048 MK464303 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Schismaderma carens BMNH 2018.5725 SL2049 MK464302 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Schismaderma carens BMNH 2018.5726 SL2050 MK464301 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Schismaderma carens BMNH 2018.5727 =SL 2051 MK464300 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Schismaderma carens BMNH 2018.5728 SL2052 MK464299 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
HEMISOTIDAE
Hemisus cf. guineensis BMNH 2018.5801 SL2252 MK464449 — Hillwood Farm -11.26690 24.31666 1308
Hemisus cf. guineensis BMNH 2018.5800 SL2110 MK464450 Lukwakwa -12.66084 24.43697 1063
Hemisus cf. guineensis BMNH 2018.5799 SL 2091 MK464451 Sioma Ngwezi NP -16.89873 23.59847 1009
Hemisus marmoratus BMNH 2018.5713 SL2018 = MK464448 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Hemisus marmoratus BMNH 2018.5714 SL2090 MK464447 Sioma Ngwezi NP -16.89873 23.59847 1009
HYPEROLIIDAE
Hyperolius dartevellei BMNH 2018.5681 SL2098 MK464446 Chavuma FR -13.07006 22.92880 1073
Hyperolius dartevellei BMNH 2018.5683 SL2139 MK464444 ~— Hillwood Farm -11.26690 24.31666 1308
Hyperolius dartevellei BMNH 2018.5684 SL2140 MK464443 ~~ Hillwood Farm -11.26690 24.31666 1308
Hyperolius dartevellei BMNH 2018.5682, SL2127 MkK464445 ~~ Lukwakwa -12.66084 24.43697 1063
Hyperolius kachalolae BMNH 2018.5676 SL2138 MK464442 ~~ Hillwood Farm -11.26690 24.31666 1308
Hyperolius kachalolae BMNH 2018.5677 = SL2149. MkK464441 ~— Hillwood Farm -11.26316 24.32782 1356
Hyperolius kachalolae BMNH 2018.5678 SL2180 MK464440 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius kachalolae BMNH 2018.5679 SL2243 MK464439 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius kachalolae BMNH 2018.5680 SL2244 MK464438 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius major BMNH 2018.5675 SL2159 MK464437 ~— Hillwood Farm -11.27444 24.32444 1416
Hyperolius marginatus BMNH 2018.5667 SL2126 MK464436 Lukwakwa -12.66091 24.42943 1100
Hyperolius marginatus BMNH 2018.5668 SL2063 MK464435 ~ Nanzila Plains, Kafue NP -16.28138 25.91676 L032
Hyperolius marginatus BMNH 2018.5674 SL2064 MK464434 = Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Hyperolius nasicus BMNH 2018.5666 SL2056 MK464433 ~ Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Hyperolius paralellus BMNH 2018.5687) = SL2133) MK464432 ~— Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5688 SL2136 MK464431 Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5689 SL2137 MK464430 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5690 SL 2141 MK464429 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5691 SL2142 MK464428 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5692, SL2150 MK464427 ~~ Hillwood Farm -11.26316 24.32782 1356
Hyperolius paralellus BMNH 2018.5693 SL2161 MK464426 ~— Hillwood Farm -11.27444 24.32444 1416
Hyperolius paralellus BMNH 2018.5694 SL2179 MK464425 — Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5695 SL2184 Hillwood Farm -11.26690 24.31666 1308
Hyperolius paralellus BMNH 2018.5696 SL2224 MK464424 = Nkwaji -11.50420 24.56456 1386
Hyperolius paralellus BMNH 2018.5697 = SL2225 MK464423 Nkwaji -11.50420 24.56456 1386
Hyperolius paralellus BMNH 2018.5698 SL2220 MK464422 Nkwaji -11.60592 24.55448 1244
Hyperolius paralellus BMNH 2018.5699 SL2240 MK464421 Nkwaji -11.53906 24.55262 1336
Hyperolius paralellus BMNH 2018.5700 SL 2241 MK464420 Nkwaji -11.53906 24.55262 1336
Hyperolius quinquevittatus BMNH 20185685 SL2216 MK464419 = Nkwaji -11.53906 24.55262 1336
Amphib. Reptile Conserv. 22 August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
Hyperolius quinquevittatus BMNH 2018.5686 SL 2217 Nkwaji -11.53906 24.55262 1336
Kassina senegalensis BMNH 2018.5810 SL2106 | MK464406 Chavuma FR -13.07006 22.92880 1073
Kassina senegalensis BMNH 2018.5802 SL2129 MK464414 Hillwood Farm -11.26690 _24,31666 1308
Kassina senegalensis BMNH 2018.5803. SL2130 MK464413 Hillwood Farm -11.26690 —_24,31666 1308
Kassina senegalensis BMNH 2018.5804. SL2223. MK464412 — Nkwaji -11.50420 24,56456 1386
Kassina senegalensis BMNH 2018.5805 SL2073 MK464411 — Sioma Ngwezi NP -16.89873 23.59847 1009
Kassina senegalensis BMNH 2018.5806 SL2074 MK464410 — Sioma Ngwezi NP -16.89873 23.59847 1009
Kassina senegalensis BMNH 2018.5807 SL2075 MK464409 — Sioma Ngwezi NP -16.89873 2359847 1009
Kassina senegalensis BMNH 2018.5808 SL2076 MK464408 — Sioma Ngwezi NP -16.89873 23.59847 1009
Kassina senegalensis BMNH 2018.5809 SL2087 MK464407_ — Sioma Ngwezi NP -16.89873 23.59847 1009
PHRYNOBATRACHIDAE
| ee ee ee BMNH 2018.5873. SL2157 | MK464397 Hillwood Farm -11.26316 24,32782 1356
i‘ eet, of BMNH 2018.5874. SL2162 MK464396 Hillwood Farm -11.27444 2432444 1416
‘ per ade cL BMNH 2018.5875 SL2163 MK464395 Hillwood Farm -11.26316 24.32782 1356
; ieee akin i eae BMNH 2018.5876 SL2164 | MK464394 Hillwood Farm -11.26316 24,32782 1356
ee o BMNH 2018.5877. SL2165 = _MK464393 Hillwood Farm -11.26316 24,32782 1356
i ited dar - BMNH 2018.5878 SL2166 MK464392 Hillwood Farm -11.26316 24.32782 1356
; ecaireteabe 7 BMNH 2018.5889 SL2120 MK464389 — Lukwakwa -12.66084 24.43697 1063
Phrynobatrachus cf. . oft sh
BMNH 2018.5879 SL2208 MK464391 = Nkwaji -11.56594. —.24.52659 1311
parvulus
Phrynobatrachus cf. : PA dae
BMNH 2018.5880 SL2210 MK464390 — Nkwaji -11.56594 —.24,52659 1311
parvulus
PRODI CE CE BMNH 2018.5882 SL 2205 Nkwaji -11.56594. 24.52659 1311
parvulus
DL yO RGIrabiRE Cl: BMNH 2018.5883 SL 2234 Nkwaji -11.56567 — 24.52605 1263
parvulus
ER vier eiey deus Ch BMNH 2018.5884 SL 2235 Nkwaji -11.56567 — 24.52605 1263
parvulus
RD ACHES, BMNH 2018.5885 SL 2236 Nkwaji -11.56567 —_24.52605 1263
parvulus
MEADE CRUSE: BMNH 2018.5886 SL 2237 Nkwaji -11.56567 — 24.52605 1263
parvulus
Hey CRO aChHis- eh. BMNH 2018.5887 SL 2238 Nkwaji -11.56567 — 24.52605 1263
parvulus
PIN RCDGI OCHS Che BMNH 2018.5888 SL 2239 Nkwaji -11.56567 — 24.52605 1263
parvulus
Pu ODER ACEUS BMNH 2018.5831 SL2010 MK464388 = Mayukuyuku, Kafue NP -14.91533 26.06311 1012
mababiensis
BN OHA, Aas BMNH 2018.5832. SL2011 = MK464387 = Mayukuyuku, Kafue NP -14.91533 26.0631 1012
mababiensis
Phrynobatrachus Es a
oe BMNH 2018.5881 SL 2015 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
mababiensis
Ripry robin achis BMNH 2018.5833 SL2065 MK464386 = Nanzila Plains, Kafue NP -16.28138 25.91676 1032
mababiensis
BP levnoparr actus BMNH 2018.5834. SL2080 MK464385 — Sioma Ngwezi NP -16.89873 23.59847 1009
mababiensis
Amphib. Reptile Conserv. 23 August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
pI BOE ET aCiES. BMNH 2018.5835 SL 2081 Sioma Ngwezi NP -16.89873 23.59847 1009
mababiensis
Phrynobatrachus natalensis BMNH 2018.5848 SL2045 MK464377 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Phrynobatrachus natalensis BMNH 2018.5849 SL2046 MK464376 _ Itezhi-Tezhi, Kafue NP -15.77340 26.0115] 1036
Phrynobatrachus natalensis +BMNH 2018.5850 SL2054 MK464375 _ Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Phrynobatrachus natalensis BMNH 2018.5853 SL2066 = MK464372 Maramba Lodge, Livingstone -17.89120 25.8582] 900
Phrynobatrachus natalensis BMNH 2018.5854 SL2067 MK464371 Maramba Lodge, Livingstone -17.89120 25.8582] 900
Phrynobatrachus natalensis BMNH 2018.5837. SL2016 MK464384 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5838 SL2017 = MK464383 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5839 SL2026 MK464382 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5840 SL2027 MK464381 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5841 SL2033 MK464380 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5842 SL2034 = MK464379 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5843 SL2037 MK464378 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5844 SL 2028 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5845 = SL 2029 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5846 — SL 2030 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5847 = SL 2031 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Phrynobatrachus natalensis BMNH 2018.5851 SL2055 MK464374 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Phrynobatrachus natalensis BMNH 2018.5852. SL2057 MkK464373 ~~ Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Phrynobatrachus sp.1 BMNH 2018.5866 SL2143 MK464364 ~— Hillwood Farm -11.26316 24.32782 1356
Phrynobatrachus sp.1 BMNH 2018.5867 SL2144 MK464363 ~~ Hillwood Farm -11.26316 24.32782 1356
Phrynobatrachus sp.1 BMNH 2018.5856 SL2195 MK464369 = Nkwaji -11.60592 24.55448 1244
Phrynobatrachus sp.1 BMNH 2018.5857. SL 2196 Nkwaji -11.60592 24.55448 1244
Phrynobatrachus sp.1 BMNH 2018.5858 SL2197 MK464368 Nkwaji -11.60592 24.55448 1244
Phrynobatrachus sp.1 BMNH 2018.5859 SL2198 = MK464367 = Nkwaji -11.60592 24.55448 1244
Phrynobatrachus sp.1 BMNH 2018.5860 SL2199 MK464366 Nkwaji -11.60592 24.55448 1244
Phrynobatrachus sp.1 BMNH 2018.5861 SL 2211 Nkwaji -11.56594 24.52659 1311
Phrynobatrachus sp.1 BMNH 2018.5862 SL 2219 Nkwaji -11.56567 24.52605 1263
Phrynobatrachus sp.1 BMNH 2018.5863 SL2232 MK464365 Nkwaji -11.56567 24.52605 1263
Phrynobatrachus sp.1 BMNH 2018.5868 SL2206 MK464362 Nkwaji -11.56594 24.52659 131]
Phrynobatrachus sp.1 BMNH 2018.5869 SL2207 MK464361 Nkwaji -11.56594 24.52659 1311
Phrynobatrachus sp.1 BMNH 2018.5870 SL2209 MK464360 Nkwaji -11.56594 24.52659 jevel
Phrynobatrachus sp.1 BMNH 2018.5871 SL2231 MK464359 = Nkwaji -11.56567 24.52605 1263
Phrynobatrachus sp.1 BMNH 2018.5872, SL2233) MK464358 Nkwaji -11.56567 24.52605 1263
Phrynobatrachus sp.2 BMNH 2018.5836 SL2071 #MK464357 Ngonye Falls Camp -16.66139 23.57280 929
Phrynobatrachus sp.2 BMNH 2018.5864 SL2095 MK464356 Sioma Ngwezi NP -16.89873 23.59847 1009
Phrynobatrachus sp.2 BMNH 2018.5865 SL2096 MK464355 Sioma Ngwezi NP -16.89873 23.59847 1009
Phrynobatrachus sp.3 BMNH 2018.5855 SL2072 MK464370 Ngonye Falls Camp -16.66139 23.57280 929
PIPIDAE
Xenopus poweri BMNH 2018.5654 SL2173 MK464274 ~— Hillwood Farm -11.26690 24.31666 1308
Xenopus poweri BMNH 2018.5655 SL2174 =MK464273 ~— Hillwood Farm -11.26690 24.31666 1308
Xenopus poweri BMNH 2018.5656 SL2175 =MK464272 ~— Hillwood Farm -11.26690 24.31666 1308
Amphib. Reptile Conserv. 24 August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
Xenopus poweri BMNH 2018.5657, = SL2176 MK464271 ~— Hillwood Farm -11.26690 24.31666 1308
Xenopus poweri BMNH 2018.5658 SL 2177 Hillwood Farm -11.26690 24.31666 1308
Xenopus poweri BMNH 2018.5659 SL2222 MK464270 = Nkwaji -11.50420 24.56456 1386
Xenopus pygmaeus BMNH 2018.5651 SL2134 MK464269 — Hillwood Farm -11.26690 24.31666 1308
Xenopus pygmaeus BMNH 2018.5652, SL2135 MK464268 — Hillwood Farm -11.26690 24.31666 1308
Xenopus pygmaeus BMNH 2018.5653 SL2156 MK464267 ~— Hillwood Farm -11.26690 24.31666 1308
PTYCHADENIDAE
Ptychadena anchietae BMNH 2018.5735 SL2040 MK464344 _ Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena anchietae BMNH 2018.5736 SL 2039 Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena anchietae BMNH 2018.5730 SL 2019 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena anchietae BMNH 2018.5731 SL2020 MK464345 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena anchietae BMNH 2018.5732 SL 2022 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena anchietae BMNH 2018.5733 SL 2023 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena anchietae BMNH 2018.5734 SL 2024 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena grandisonae BMNH 2018.5737. = SL2214 MK464318 Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5738 SL 2215 Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5739 SL2226 MK464317 = Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5740 SL2227 MK464316 Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5741 SL2228 MK464315 = Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5742 SL2229 MK464314 = Nkwaji -11.5042 24.56456 1386
Ptychadena grandisonae BMNH 2018.5743, SL2230 MK464313 Nkwaji -11.5042 24.56456 1386
Ptychadena cf. guibei BMNH 2018.5764 SL2035 MK464324 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena cf. guibei BMNH 2018.5765 SL2079 MK464323 Sioma Ngwezi NP -16.89873 23.59847 1009
Ptychadena mapacha BMNH 2018.5772 SL2014 MK464312 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena cf. mossambica BMNH 2018.5754 SL2042 MK464342 _ Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena cf. mossambica BMNH 2018.5755 = SL2043. MK464341 _ Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena cf. mossambica BMNH 2018.5756 SL2044 MK464340 — Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena cf. mossambica BMNH 2018.5757. =SL2038 MK464339 Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena cf. mossambica =BMNH 2018.5763 = SL 2021 MK464336 = Mayukuyuku, Kafue NP -14.91533 26.06311 1012
Ptychadena cf. mossambica BMNH 2018.5758 SL 2088 Sioma Ngwezi NP -16.89873 23.59847 1009
Ptychadena cf. mossambica BMNH 2018.5759 SL2089 MK464338 Sioma Ngwezi NP -16.89873 23.59847 1009
Ptychadena cf. mossambica + BMNH 2018.5760 SL2094 MK464337 Sioma Ngwezi NP -16.89873 23.59847 1009
Ptychadena cf. mossambica ~=BMNH 2018.5761 Sioma Ngwezi NP -16.89873 23.59847 1009
Ptychadena cf. mossambica BMNH 2018.5753. SL 2041 Itezhi-Tezhi, Kafue NP -15.7734 26.01151 1036
Ptychadena nilotica BMNH 2018.5781 SL 2068 =MK464327 Maramba Lodge, Livingstone -17.8912 25.85821 900
Ptychadena nilotica BMNH 2018.5773 = SL2058 MK464332 = Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5774 SL2059 MK464331 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5775 SL2061 MK464330 ~ Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5776 SL 2062 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5777, =SL2278 MK464329 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5778 = SL 2279 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5779 = SL2280 MK464328 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena nilotica BMNH 2018.5780 SL 2281 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Amphib. Reptile Conserv. 25 August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
Ptychadena obscura BMNH 2018.5768 SL2155 MK464322 ~— Hillwood Farm -11.2669 24.31666 1308
Ptychadena obscura BMNH 2018.5766 SL2131 MK464311 = Hillwood Farm -11.2669 24.31666 1308
Ptychadena obscura BMNH 2018.5767 = SL2132 MK464310 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena oxyrhynchus BMNH 2018.5783 SL2250 #MK464325 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena oxyrhynchus BMNH 2018.5782. SL2060 MK464326 = Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ptychadena porosissima BMNH 2018.5769 SL2158 = MK464321 — Hillwood Farm -11.27531 24.31977 1340
Ptychadena porosissima BMNH 2018.5770 SL2168 = MK464320 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena porosissima BMNH 2018.5771 SL2248 = MK464319 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena cf. taenioscelis |» BMNH 2018.5784 SL2169 MK464335 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena cf. taenioscelis = BMNH 2018.5785 SL 2171 MK464334 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena cf. taenioscelis © BMNH 2018.5786 SL2172 MK464333 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena upembae BMNH 2018.5750 SL2154. MK464348 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena upembae BMNH 2018.5751 SL2170 MK464347 ~— Hillwood Farm -11.2669 24.31666 1308
Ptychadena upembae BMNH 2018.5752. SL 2251 MK464346 — Hillwood Farm -11.2669 24.31666 1308
Ptychadena upembae BMNH 2018.5744 SL2192 MK464354 Nkwaji -11.60592 24.55448 1244
Ptychadena upembae BMNH 2018.5745 SL2193 MK464353 Nkwaji -11.60592 24.55448 1244
Ptychadena upembae BMNH 2018.5746 SL2194 MK464352 Nkwaji -11.60592 24.55448 1244
Ptychadena upembae BMNH 2018.5747 SL2212 MK464351 Nkwaji -11.56594 24.52659 1311
Ptychadena upembae BMNH 2018.5748 SL2218 MK464350 Nkwaji -11.53906 24.55262 1336
PyxICEPHALIDAE
Amietia chapini BMNH 2018.5660 SL2186 MK464482 ~~ Hillwood Farm -11.26690 24.31666 1308
Amietia chapini BMNH 2018.5661 SL2185 MK464481 — Hillwood Farm -11.26690 24.31666 1308
Amietia chapini BMNH 2018.5662 SL2178 Hillwood Farm -11.26690 24.31666 1308
Amietia chapini BMNH 2018.5663 SL2183 MK464480 — Hillwood Farm -11.26690 24.31666 1308
Amietia chapini BMNH 2018.5664 SL2151 Hillwood Farm -11.26690 24.31666 1308
Amietia chapini BMNH 2018.5665 SL 2167 Hillwood Farm -11.26690 24.31666 1308
Pyxicephalus cf. adspersus BMNH 2018.5787 SL2077 MK464309 Sioma Ngwezi NP -16.89873 23.59847 1009
Pyxicephalus cf. adspersus BMNH 2018.5788 SL2082 MK464308 Sioma Ngwezi NP -16.89873 23.59847 1009
Pyxicephalus cf. adspersus BMNH 2018.5789 SL2083 MK464307 Sioma Ngwezi NP -16.89873 23.59847 1009
Pyxicephalus cf. adspersus BMNH 2018.5790 SL2084 MK464306 Sioma Ngwezi NP -16.89873 23.59847 1009
Pyxicephalus cf. adspersus BMNH 2018.5791 SL2097 MK464305 Sioma Ngwezi NP -16.89873 23.59847 1009
Tomopterna marmorata BMNH 2018.5792 SL2070 MK464287 Maramba Lodge, Livingstone -17.89120 25.85821 900
Tomopterna sp. BMNH 2018.5793 SL2078 MK464286 Sioma Ngwezi NP -16.89873 23.59847 1009
Tomopterna sp. BMNH 2018.5794 SL2085 MK464285 Sioma Ngwezi NP -16.89873 23.59847 1009
Tomopterna sp. BMNH 2018.5795 SL2086 MK464284 Sioma Ngwezi NP -16.89873 23.59847 1009
Tomopterna sp. BMNH 2018.5796 SL2092 MK464283 Sioma Ngwezi NP -16.89873 23.59847 1009
Tomopterna sp. BMNH 2018.5797 SL2093 MK464282 Sioma Ngwezi NP -16.89873 23.59847 1009
RHACOPHORIDAE
Chiromantis xerampelina BMNH 2018.5798 SL 2036 MK464456 Mayukuyuku, Kafue NP -14.91533 26.06311 1012
REPTILIA: SQUAMATA
AGAMIDAE
Agama armata BMNH 2018.2751 SL2253 MK464483 Negonye Falls Camp -16.66139 23.57280 929
Amphib. Reptile Conserv. 26 August 2019 | Volume 13 | Number 2 | e181
Bittencourt-Silva
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
CHAMAELEONIDAE
Chamaeleo dilepis BMNH 2018.2755 SL2099 MK464458 Chavuma FR -13.07006 22.92880 1073
Chamaeleo dilepis BMNH 2018.2756 SL2100 MK464457. Chavuma FR -13.07006 22.92880 1073
COLUBRIDAE
Crotaphopeltis hotamboeia BMNH 2018.2773 SL2247 MK464455__ Hillwood Farm -11.26690 24.31666 1308
Crotaphopeltis hotamboeia BMNH 2018.2776 SL2272 Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Crotaphopeltis hotamboeia BMNH 2018.2777. SL2258 MK464454_ — Sioma Ngwezi NP -16.89873 23.59847 1009
i a Se BMNH 2018.2772 SL2249 = MK464304 Hillwood Farm -11.26690 _24,31666 1308
Philothamnus hoplogaster | BMNH 2018.2775 SL2277 + MK464398 _ Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Thelotornis kirtlandii BMNH 2018.2760 SL 2182 Hillwood Farm -11.26690 24.31666 1308
GEKKONIDAE
Hemidactylus mabouia BMNH 2018.2740 SL 2264 Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Hemidactylus mabouia BMNH 2018.2742 $SL2263 MK464452 __Itezhi-Tezhi, Kafue NP -15.77340 2601151 1036
Hemidactylus mabouia BMNH 2018.2741 SL2276 MK464453 —Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Lygodactylus angolensis BMNH 2018.2766 SL2213 MK464405— Nkwaji -11.52743 _ 24,53532 1343
Lygodactylus angolensis BMNH 2018.2767 SL2187 MK464404— Nkwaji -11,60592 _24.55448 1244
Lygodactylus chobiensis BMNH 2018.2743. SL2267 MK464403 __Itezhi-Tezhi, Kafue NP -15.77340 2601151 1036
Lygodactylus chobiensis BMNH 2018.2744 SL 2268 Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Pachydactylus punctatus | BMNH 2018.2757 SL2265 = MK464400 __Itezhi-Tezhi, Kafue NP -15.77340 2601151 1036
Pachydactylus punctatus BMNH 2018.2758 SL 2266 Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
Pachydactylus punctatus BMNH 2018.2759 SL 2269 Itezhi-Tezhi, Kafue NP -15.77340 26.01151 1036
GERRHOSAURIDAE
Gerrhosaurus bulsi BMNH 2018.2754. SL2181 Hillwood Farm -11.26690 24.31666 1308
LACERTIDAE
Ichnotropis capensis BMNH 2018.2746 SL2103 MK464417. Chavuma FR -13.07006 22.92880 1073
Ichnotropis capensis BMNH 2018.2747. SL2260 MK464416 ~~ Lukwakwa -12.66084 24.43697 1063
Ichnotropis capensis BMNH 2018.2749 = SL 2259 Lukwakwa -12.66084 24.43697 1063
Ichnotropis capensis BMNH 2018.2748 SL 2274 Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ichnotropis capensis BMNH 2018.2750 SL2273. MK464415_—_Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Ichnotropis capensis BMNH 2018.2745 SL2256 MK464418 — Sioma Ngwezi NP -16.89873 23.59847 1009
Meroles squamulosus BMNH 2018.2753. SL2275 MK464401 _—Nanzila Plains, Kafue NP -16.28138 25.91676 1032
Meroles squamulosus BMNH 2018.2752 SL2257 MK464402 —‘ Sioma Ngwezi NP -16.89873 23.59847 1009
LAMPROPHIIDAE
Atractaspis congica BMNH 2018.2274. SL2160 | MK464459 Hillwood Farm -11.27444 24,32444 1416
SCINCIDAE
Typhlacontias rohani BMNH 2018.2761 SL2254. MK464275 nee ate ee erSioMma 1476966053. 83356743 999
Panaspis cf. wahlbergi BMNH 2018.2738 SL2101 MK464399 Chavuma FR -13.07006 — 22.92880 1073
Panaspis cf. wahlbergi BMNH 2018.2739 SL 2104 Chavuma FR -13.07006 22.92880 1073
ae oe BMNH 2018.2762 SL2270 MK464281 _ Itezhi-Tezhi, Kafue NP -15.77340 26.0115] 1036
ph eS BMNH 2018.2763 SL 2032 Mayukuyuku, Kafue NP -14.91533 26.0631 1012
Amphib. Reptile Conserv. 27 August 2019 | Volume 13 | Number 2 | e181
Herpetological survey of western Zambia
Appendix 1 (continued). List of amphibians and reptiles found in western Zambia, including species vouchers, GenBank accession
numbers, and locality information. Museum acronym: BMNH — Natural History Museum, London, United Kingdom. GPS datum WGS-84.
Species Voucher ID Field ID GenBank Locality Latitude Longitude Altitude
Praclylepicch BMNH 2018.2765 SL2013 MK464280 Mayukuyuku, Kafue NP -14.91533 2606311 1012
albopunctata
Trachylepis damarana BMNH 2018.2764 SL2255 | MK464279 Rae Cs OFSHOMAS 9 1666953 2956743 999
Trachylepis wahlbergii BMNH 2018.2769 SL2271 MK464278 __Itezhi-Tezhi, Kafue NP -15.77340 26.0115] 1036
Trachylepis wahlbergii BMNH 2018.2768 SL 2262 Lukwakwa -12.66084 24.43697 1063
Trachylepis wahlbergii BMNH 2018.2770 SL2261 MK464277.— Lukwakwa -12.66084 24.43697 1063
Trachylepis wahlbergii BMNH 2018.2771 SL2188 | MK464276 = Nkwaji -11.60592 24,.55448 1244
REPTILIA: Testudines
TESTUDINIDAE
Kinixys spekii No voucher Ne Nkwaji -11.53906 24.55262 1336
voucher
Amphib. Reptile Conserv. 28 August 2019 | Volume 13 | Number 2 | e181
Amphibian & Reptile Conservation
13(2) [Special Section]: 29-41 (e182).
Official journal website:
amphibian-reptile-conservation.org
Hiding in the bushes for 110 years: rediscovery of an
iconic Angolan gecko (Afrogecko ansorgii Boulenger,
1907, Sauria: Gekkonidae)
12.5.*xPedro Vaz Pinto, ‘Luis Verissimo, and **William R. Branch
'Fundagao Kissama, Rua 60 Casa 560, Lar do Patriota, Luanda, ANGOLA *CIBIO/InBio — Centro de Investigacao em Biodiversidade e Recursos
Genéticos, Universidade do Porto, Campus Agrario de Vairdo, 4485-661, Universidade do Porto, PORTUGAL °Port Elizabeth Museum (Bayworlad),
P.O. Box 13147, Humewood 6013, SOUTH AFRICA *Research Associate, Department of Zoology, P.O. Box 77000, Nelson Mandela University, Port
Elizabeth 6031, SOUTH AFRICA (deceased 14 October 2018) °>TwinLab CIBIO-ISCED, Instituto Superior de Ciéncias da Educagdo da Huila, Rua
Sarmento Rodrigues s/n, Lubango, ANGOLA
Abstract.—Boulenger (1907) described a new gecko ‘Phyllodactylus’ ansorgii based on two adult females
from ‘Maconjo, Benguella, Angola,’ but subsequent taxonomic reviews of leaf-toed geckos ascribed southern
African lineages to new genera and this species has since been tentatively placed under ‘Afrogecko.’ For over
110 years the type locality remained a mystery, and the gecko became a lost icon of Angolan herpetology.
Early searches for the gecko were confounded by misinterpretation of the type locality ‘Maconjo,’ which it is
now evident was confused with a toponym that is a well-known historical locality. Following the discovery of
new material in coastal Benguela, an examination of historical documents and cartographic material allowed
the original collecting area for the type material to be identified. Specific surveys in this area resulted in the
collection of topotypic material and the recording of behavioral observations and notes on the ecology of the
species. Afrogecko ansorgiiis a slender, gracile, and arboreal gecko that inhabits small bushy trees, particularly
blackthorn (Senegalia mellifera subsp. detinens), in the arid coastal scrubland of the Benguela coastal region.
All A. ansorgii have been found in or nearby blackthorn in which the activity of termites (Kalotermitidae) has
created hollow stems in which the geckos shelter. The type locality for Phyllodactylus (= Afrogecko) ansorgii
Boulenger, 1907 and Mabuia (= Trachylepis) laevis Boulenger, 1907, both described at the same time from
‘Maconjo, Benguella’ is accordingly restricted, and topotypic material for the latter species was also obtained.
Key Words. Ansorge, blackthorn, Kaokoveld, Maconjo, Reptilia, type locality, Trachylepis laevis
Resumo.—Boulenger (1907) descreveu a nova osga ‘Phyllodactylus’ ansorgii a partir de duas fémeas
oriundas de ‘Maconjo, Benguella, Angola,’ mas subsequentes revisOes taxonomicas das osgas-de-dedos-de-
folha fez corrresponder a novos géneros as linhagens da Africa austral e desde entao esta espécie tem sido
tentativamente incluida em ‘Afrogecko.’ Durante mais de 110 anos a localidade tipica permaneceu um misteério,
e a osga tornou-se um icone perdido da herpetologia Angolana. Buscas iniciais pela osga ficaram baralhadas
devido a uma ma interpretacao da localidade tipica ‘Maconjo,’ que é hoje evidente ter sido confundida com
um toponimo que é uma localidade historica bem conhecida. Apos a descoberta de novo material na regiao
costeira de Benguela, a despistagem de documentos historicos e material cartografico permitiu identificar
a area de colheita original do material tipico. Levantamentos especificos nesta area resultaram na colheita
de material topotipico e no registo de observagoes comportamentais e notas sobre a ecologia da espécie. O
Afrogecko ansorgii € uma osga delgada, delicada e arboricola que habita pequenas arvores de porte arbustivo,
particularmente espinheiras (Senegalia mellifera subsp. detinens), nas estepes aridas arbustivas da regiao
costeira de Benguela. Todos os A. ansorgii foram encontrados nestas espinheiras ou na sua vizinhanga, e onde
a actividade de termitas (Kalotermitidae) gerou talos ocos onde as osgas se abrigam. A localidade tipica para o
Phyllodactylus (= Afrogecko) ansorgii Boulenger 1907 e para o Mabuia (= Trachylepis) laevis Boulenger 1907,
ambos descritos na mesma altura para ‘Maconjo, Benguella’, é desta forma restringida, e material topotipico
da ultima espécie foi tambem obtido.
Palavras-chave: Reptilia, localidade tipica, Maconjo, Ansorge, espinheira, Kaokoveld, Trachylepis laevis
Citation: Vaz Pinto P, Luis Verissimo L, Branch WR. 2019. Hiding in the bushes for 110 years: rediscovery of an iconic Angolan gecko (Afrogecko
ansorgii Boulenger, 1907, Sauria: Gekkonidae). Amphibian & Reptile Conservation 13(2) [Special Section]: 29-41 (e182).
Copyright: © 2019 Vaz Pinto et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Submitted: 12 March 2019; Accepted: 14 March 2019; Published: 11 August 2019
Correspondence. * pedrovazpinto@gmail.com
Amphib. Reptile Conserv. 29 August 2019 | Volume 13 | Number 2 | e182
Rediscovery of Afrogecko ansorgii in Angola
Introduction
The biodiversity of Angola, and particularly that of the
herpetofauna, is acknowledged to be inadequately known
(Branch 2016; Huntley and Ferrand 2019). This was
not always the case, and like many countries in Africa
the early phase of colonial exploration and settlement
resulted in the discovery of numerous novel animals.
For almost 50 years (1866-1915) these collections were
sent to European museums for study and description, and
they stimulated much scientific interest. Early studies on
the Angolan herpetofauna were numerous, particularly
those of José Vicente Barbosa du Bocage, the father of
Angolan herpetology. His monographic Herpétologie
d’Angola et du Congo (Bocage 1895) remained for
over a century the definitive synthesis of the country’s
herpetofauna, until the recent publication of a historic
herpetological atlas (Marques et al. 2018). Currently,
studies on the herpetofauna of Angola are entering a
new phase following the closure of protracted hostilities
at the end of the colonial era. Recent field surveys (e.g.,
Huntley 2009; Ernst et al. 2014; Huntley and Francisco
2015; Ceriaco et al. 2016, 2018; Conradie et al. 2016)
have uncovered new species of amphibians (Conradie
et al. 2012a, 2013; Ceriaco et al. 2018) and reptiles
(Conradie et al. 2012b; Stanley et al. 2016). However,
a number of important historical species described
during the colonial period still remain known from only
their original description, e.g., Sepsina copei Bocage,
1866 and Cordylus angolensis (Bocage 1895), or only
a few subsequent specimens, e.g., Monopeltis luandae
Gans 1976 (Branch et al. 2018), Psammophis ansorgii
Boulenger 1905, and Psammophylax ocellatus Bocage
1873 (Branch et al. 2019a). Tragically, much of the
historical material studied by Bocage, including almost
all of his type material, was lost in the fire that destroyed
the Museu Bocage collections in 1978.
Perhaps the most iconic of the ‘lost’ Angolan species
is Ansorge’s Leaf-toed Gecko, which was described by
Boulenger (1907) as Phyllodactylus ansorgii, over 110
years ago. Leaf-toed geckos have a globally wide-ranging
distribution and all of them used to be included within
Phyllodactylus until a comprehensive review performed
by Bauer (1997) ascribed the southern African species to
three new genera. The genus Afrogecko initially included
two species found in South Africa, A. porphyreus, and
A. swartbergensis, and two Angolan leaf-toed geckos, A.
plumicaudus and A. ansorgii (Bauer 1997; Haacke 2008).
However, more recent phylogenetic studies revealed
deeply independent evolutionary histories among these
lineages, leading A. swartgergensis and A. plumicaudus
to be transferred to the new monotypic genera Ramigekko
and Kolekanos, respectively, while due to the lack of
available material ansorgii was provisionally maintained
within Afrogecko (Heinicke et al. 2014).
The species description was based on two female
specimens from Maconjo, Benguella (now Benguela)
collected by Dr. W.J. Ansorge on one of his Angolan
journeys, between 1903 and 1906, and the types, BMNH
1946.8.24.52—53, were deposited in the Natural History
Museum London (United Kingdom). The exact locality
Amphib. Reptile Conserv.
of Ansorge’s Maconjo has caused confusion, and
erroneous interpretation of its whereabouts probably
delayed the species’ rediscovery. Moreover, the species
is now known to live in an unusual habitat, and this may
have also led to it being overlooked. Crawford-Cabral
and Mesquitela (1989) summarized all known localities
for Angolan terrestrial vertebrates and considered
Maconjo a variant spelling of Maconge, an old farm
situated in Namibe Province, formerly Mossamedes (=
Mocamedes) District (15°01’S, 13°12’E, 700 m asl).
Maconjo, Mossamedes features as a collecting locality
for reptiles in the 19" century for the famous Portuguese
collector José de Anchieta (de Andrade 1985), and in his
monograph Bocage (1895) recorded numerous reptiles
from Maconjo, Mossamedes, including: the terrapin
Pelomedusa galeata (= P. subrufa); the lacertids Nucras
tessellata and Eremias lugubris (= Heliobolus lugubris),
the rupicolous skink Mabuia chimbana (= Trachylepis
chimbana);, the python Python natalensis, the snakes
Prosymna_ frontalis (= P. angolensis, fide Broadley
1980), Psammophylax nototaenia (= Hemirhaggheris
viperina, fide Broadley 2000), Psammophis sibilans (=
P. subtaeniatus), Elapsoidea guentheri var. semiannulata
(= E. s. semiannulata), and Causus resimus. Many of
these have been subsequently recorded in the region
(data not shown).
A farm and stream at the base of the Humpata plateau
near Leba Pass are called Maconjo on old maps and lie
in the vicinity of the old Portuguese fort of Capangombe,
which dates from the mid-nineteenth century and marks
the route for some of the earliest inland incursions of
colonists in southern Angola. This locality was then
included in the District of Mossamedes. However,
Boulenger referred the gecko’s type locality to “Maconjo,
Benguella,’ placing it in Benguela instead of Mossamedes
District. This suggests either that it was ascribed by
Ansorge to the wrong district, or that there could exist
two different sites bearing the name Maconjo. It should
be noted that mistaking Mossamedes for Benguela would
have been unlikely in the early 20" century, when both
districts were well established and had been for some
time. They have also remained as separate administrative
entities ever since. Yet this incongruence seems to have
gone unnoticed, and it appears that most subsequent
researchers have considered there was only one Maconjo,
and the references to different provinces, Mossamedes (=
Namibe) or Benguela, were either ignored or taken as
synonyms (Bauer etal. 1997; Heinicke et al. 2014; Ceriaco
et al. 2016; Uetz et al. 2018). The accepted wisdom that
there was only one Maconjo, and that it was situated
below the escarpment in the current Namibe Province,
resulted in numerous unsuccessful searches for the
gecko around Capangombe by various researchers from
1974 to 2016. More recently, Maconjo was tentatively
synonymized with another well-known collecting site
in southwestern Angola ‘Fazenda Mucungo’ (Marques
et al. 2018), however, no further details were provided
to justify the new locality. Mucungo also lies on the
coastal plain of Namibe and therefore cannot resolve the
geographical discrepancies.
Another species from ‘Maconjo’ that Boulenger
(1907) described from the same Ansorge collection
August 2019 | Volume 13 | Number 2 | e182
Vaz Pinto et al.
was the small rupicolous skink Mabuia (= Trachylepis)
laevis, commonly called the Angolan Blue-tailed Skink
(Tf. laevis). It is rupicolous, sheltering in thin cracks in
hard, fractured rocks and has numerous morphological
adaptations to this habitat (Paluh and Bauer 2017).
Despite its conspicuous coloration, the species has
only rarely been collected in Angola after the original
description (Boulenger 1907). Laurent (1964) recorded
a male from Munhino, 50 km W of Lubango, and
Hellmich (1957) reported a problematic specimen from
Piri-Dembos (= Piri) that should be treated with caution
(Laurent 1964; Ceriaco et al. 2016). The Angolan Blue-
tailed Skink was recently recorded from granite outcrops
50 km east of Namibe (W.R. Branch, pers. comm.), and
just north of Tambor near Iona National Park (Ceriaco et
al. 2016), and additional material has been collected in
northern Namibe Province, at Chapéu Armado, Serra da
Neve, and Lola by the authors of the current study. Still,
the most significant collections of 7’ /aevis were made
by Wulf Haacke during an expedition to southwestern
Angola in 1971, when he collected 18 specimens from
Tambor and other localities in Namibe Province (all
deposited in the Ditsong Natural History Museum,
Pretoria, South Africa). In addition, and importantly, he
collected the first records since Ansorge from Benguela
Province, with material from 35 km south of Dombe
Grande and 53 km south of Benguela.
Until now, no additional material for A. ansorgii had
ever been collected, despite searches by experienced
herpetologists in the 1970s and after 2009. In this paper
we report on finding the species and obtaining new
material that includes the first male specimens. The
type locality is here confidently restricted, and topotypic
material was collected for both A. ansorgii and T. laevis.
In addition, by collecting the gecko on a second site, we
extend its known range by about 100 km. Behavioral
and habitat observations were also recorded, and provide
useful insights into their unique ecological requirements.
Materials and Methods
To investigate local toponyms and locate the type
locality, historical cartographic material was thoroughly
examined and, in the absence of available diaries for Dr.
Ansorge’s Angolan journeys, we consulted a remarkable
manuscript by the American ornithologist James Chapin
which provides a detailed summary of Ansorge’s
itineraries in Angola (Chapin, undated).
After first encountering A. ansorgii, we conducted
a series of additional field trips in search of the gecko
between November 2016 and June 2018, to five different
sites, including the restricted type locality and additional
locations where we looked for their presence. The surveys
included mostly nocturnal searches, and daytime habitat
observations. A total of 23 specimens of A. ansorgii
were collected in two sites, including the restricted type
locality. All specimens were photographed in life, and
subsequently preserved in formalin. Collected specimens
were deposited at Port Elizabeth Museum (PEM R23907—
23916), at ISCED — Instituto Superior de Ciéncias da
Educacdo da Huila (NB603-605; NB822-—826) and at
Kissama Foundation (KFH0007—0010). Additionally,
Amphib. Reptile Conserv.
31
behavioral observations were also recorded by locating
the geckos at night with flashlights and observing their
foraging habits, and by confirming their daytime shelters.
Reptile species lists were compiled for each site visited,
and topotypic material was also secured for 7: /aevis,
with one specimen collected and deposited at Kissama
Foundation collection (FKH0018).
Results
Type locality: From Chapin’s summary it is apparent
that Ansorge visited ‘Makonjo, Benguella’ on 7 July
1904. Chapin used the spelling ‘Makonjo’ instead of
following Boulenger’s ‘Maconjo,’ but the use of a ‘k’
or ‘c’ 1s often interchangeable when applied to Angolan
toponymy. To avoid continued confusion with toponyms
we hereafter keep the spelling as Maconjo and add the
district/province name when relevant. Ansorge left the
locality of “‘Huxe, Benguella’ (= Uche, 12°44’S, 13°21’E,
250 m asl) on the previous day on his way to Benguela’s
sandpits and the town of Catengue (13°02’S, 13°44’E,
550 m asl), which he reached on 11 July 1904. This route,
depicted on a map included in the manuscript, places the
locality of Maconjo clearly in Benguela as opposed to
Namibe’s coastal plain, and within a few days travel on
foot from Benguela town. In addition, there are no other
records of localities of similar spelling in the manuscript,
and no suggestion that Ansorge ever visited Capangombe
region. Moreover, based on Chapin’s document it appears
that Ansorge never descended the escarpment from the
Humpata plateau, and although he referred to his 1906
route south of Caconda as being in Mossamedes District,
Chapin failed to recognize the then newly created Huila
District. As a result, there is no evidence to suggest
that Ansorge even collected in the former Mossamedes
District as it was defined in his time, and which broadly
corresponds to the current Namibe Province.
Comparing Chapin’s notes with cartographic material
allowed the reconstruction of Ansorge’s probable route
(Fig. 1) and the identification along it of a region by
the name of ‘Conjo’ (12°53’S, 13°24’E) in Benguela
Province. This area, approximately 20 km south of Uche
and on the route towards Catengue, lies between 300
and 450 m asl, and includes two small north-flowing dry
sandy streams named respectively as “Conjo’ and ‘Conjo
Pequeno,’ both tributaries to another ephemeral stream
named ‘Cocumba.’ The region is in Benguela’s coastal
plain and would be realistically within one-day’s reach
from Uche on foot, and enroute to Catengue, making
it extremely likely that it corresponds to the true type
locality of “Maconjo, Benguela’ as recorded by Ansorge
(in Boulenger 1907). Interestingly, in the local language
Conjo means spoor and the prefix ‘Ma-’ is commonly
used to signify plurality, so the toponymy Maconjo
can be appropriately interpreted as ‘the site of various
Conjos’ or ‘site of many spoor.’
On the basis of Chapin’s notes and cartographic
material we here restrict the type locality of Phyllodactylus
(= Afrogecko) ansorgii and Mabuia (= Trachylepis) laevis,
both described by Boulenger (1907) from ‘Maconjo,
Benguella,’ to the vicinity of the streams Conjo, Conjo
Pequeno, and Cocumba (12°52’S, 13°21’E, 355 m asl),
August 2019 | Volume 13 | Number 2 | e182
Rediscovery of Afrogecko ansorgii in Angola
* Type locality - Maconjo, Benguela
—-=—- Ansorge Routes, 1904 to1906, in SW Angola
@ Newsite - sta. Maria
@ = Additional surveyed sites
—--- Angola Administratrive Districts in 1905
Fig. 1. Travel routes in Angola by Dr. Ansorge between 1904
and 1906, as per Chapin’s manuscript. Former district (broadly
corresponding to current provinces) borders are shown, as well
as collecting sites and other relevant localities.
20 km south of Uche, Benguela Province, Angola (Fig.
1). Both species, Afrogecko ansorgii and Trachylepis
laevis, were collected at this site (see below).
Rediscovery: The gecko was first rediscovered 135 km
southwest of Benguela town on 12 November 2016. The
site is located about three km from the Lucira-Benguela
road, at the head of a valley leading down to Cape Sta
Maria, Benguela Province (13°31’S, 12°38’E, 288 m
asl). The locality is ca. 185 km northwest of Maconjo,
Namibe, and ca. 100 km southwest of the type locality
in Benguela Province (Fig. 1). A total of 10 specimens
were collected at night whilst foraging in the branches of
thorny bushes (Fig. 2), mainly of blackthorn Senegalia
mellifera detinens. Subsequently, three additional
specimens were collected, and nine others observed in
the same habitat and under similar circumstances, at two
other nearby sites surveyed five km and three km to the
northwest, on 12—13 July 2017 and 11-12 August 2017,
respectively. Most specimens were located at night on
bushes situated at the base or mid-slopes of granitic hills,
and although a few were observed in various species of
small trees, the majority were found among the spiny
branches of blackthorn bushes. One specimen was found
during the day sheltering inside a hollow blackthorn
branch (Fig. 3A).
After the cartographic identification of the potentially
true type locality, specific visits to the Conjo area to
search for geckos were made on 25—26 November 2017
Amphib. Reptile Conserv.
32
and 5 December 2017. The region surveyed was located
approximately half-way between the towns of Benguela
(35 km) and Catengue (47 km) and five km south of the
small village of Talamajamba. As it shared some features
with sites at Sta Maria, although lacking in rocky habitat
suitable for Trachylepis laevis, we first focused on a site
located on a sand road that crosses the Cocumba dry
stream and runs a few hundred meters parallel to the east
of Conjo Pequeno (12°54’3S, 13°24’E, 395 m asl). The
searches resulted in our obtaining topotypic material and
further observations. Broadening the search, additional
visits on 12-13 March 2018 and 5 June 2018, focused
on an area around three isolated granite outcrops present
along the stream Cocumba and a mere 500 m west of the
confluence with stream Conjo (12°52’S, 13°21’E, 355 m
asl). Although the Cocumba is a dry stream on a semi-
desert environment, local pastoralists have long dug
artisanal wells to gain access to water on the river bed
at the base of the granite outcrops. The presence of these
wells on the confluence of Conjo and Cocumba streams
offers a realistic scenario for the site ‘Maconjo’ to have
been used as a stopover locality between Benguela
and Catengue by Ansorge in 1904. Here, additional
specimens of A. ansorgii were found in nearby bushes,
and a specimen of 7: /aevis was collected in the granite
outcrops, constituting the first topotypic material for this
species.
At Maconjo, a total of 10 specimens of A. ansorgii
were collected and 14 additional individuals were
observed foraging at night in bushes over the four visits,
mostly found in Senegalia mellifera detinens, but also
in Terminalia prunioides, Commiphora cf. africana, and
Salvadora persica, and once on a dry grass stem. Most
geckos were spotted in the early evening (approximately
between 19h00 and 21h00) in small branches 1-2 m
above ground. One specimen was observed partially
exiting a hollow blackthorn branch shortly after sunset,
as exemplified in a photograph (Fig. 3B).
Three additional coastal sites (Fig. 1) were also
surveyed in search of the geckos, one was an intermediate
location between Maconjo and Sta Maria, at Chimalavera
Regional Park (12°50’S, 13°10’E, 255 m asl), on a sandy
plateau over an east-facing limestone ridge, Benguela
Province; another ca. 35 km south of Maconjo and near
the Coporolo River (13°12’S, 13°25’E, 380 m asl); and
one further south at 17 km W of Chicambi Village, on
sandy flats with a granite ridge, in Namibe Province
(13°55’S, 12°41’E, 531 m asl). In these sites the habitat
was similar to that at Cape Sta Maria, with numerous
Senegalia mellifera detinens bushes on sandy soil and
with adjacent rock outcrops. However, in all these three
cases the blackthorn bushes lacked hollow branches and
no geckos were observed during nocturnal searches.
Habitat observations: On the vegetation map of
Angola, Barbosa (1970) defines a very extensive region
as semi-desert coastal steppe, starting as a narrow coastal
strip around 11° south, then becoming broader inland
towards the southern border with Namibia. However,
this is a very wide and rough classification and includes a
transition from dry spiny savannahs dominated by acacias
(Senegalia spp.) to mopane woodlands characterized
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Vaz Pinto et al.
Fig. 2. Afrogecko ansorgii: adult male, PEM R23907 (in life). (A) Whole body on small branch of Senegalia mellifera detinens with
epiphytic lichen. (B) Close up of head of same adult male. (C) Afrogecko ansorgii: adult female, PEM R23912 (in life) on small
branch of Senegalia mellifera detinens. (D) Close up of head of same adult female. Note elongate, subcylindrical body, relatively
short cylindrical tail that is shorter than SVL and partially prehensile, long toes with expanded terminal scansors, predominantly
dark brown dorsal coloration, and dorsolateral series of irregular pale blotches that extend on to the tail.
by the dominance of Colophospermum mopane. Still,
he refers to the arid regions near Benguela as being
characterized by an abundance of Senegalia mellifera
detinens, Senegalia spp., Salvadora persica, Euphorbia
spp., and Boscia spp. (Barbosa 1970) which likely
correspond to the more relevant areas for Ansorge’s
Gecko.
At Maconjo, Benguela, the restricted type locality,
the terrain is relatively flat, with sandy soils, irregularly
interspersed with small granitic rocks, and with a few
isolated granite outcrops at the Cocumba stream (Fig.
4A). The vegetation was relatively dense and diverse, the
trees often in close proximity or touching, but with low
canopies and not growing larger than the size of a bush
(Fig. 4B). The dominant tree/bush species were Senegalia
mellifera detinens and Terminalia prunioides, but other
species also found to be common were Commiphora cf.
africana, Boscia microphylla, Vachellia reficiens, and
Salvadora persica. Succulents were also recorded, notably
the conspicuous Aloe littoralis, plus a few Hoodia cf.
parviflora and the invasive Opuntia ficus-indica.
The Sta Maria site is situated at a slightly lower
elevation, being closer to the coast and further south than
the type locality, and in a more arid coastal environment.
It possibly receives lower rainfall, but this may be
Amphib. Reptile Conserv.
compensated for by the higher incidence of coastal fog
which is a feature of the whole Namib Desert coastline
(Cermak 2012). The effect of regular fogs, which may
extend well inland, is evident in the local abundance of
lichens that often cover the branches of bushes (Figs. 2A,
4C). At this locality the vegetation was much sparser than
at Maconjo, Benguela, particularly in the sandy valleys,
but the topography was often much more varied with
large granite boulders and steep granitic hills (Fig. 4D).
Senegalia mellifera detinens was the most abundant tree,
while other common species recorded were Salvadora
persica, Commiphora multijuga, Phaeoptilum spinosum,
and Jerminalia prunioides.
A striking find that appears positively linked with the
occurrence of the gecko is the existence in both sites of
abundant hollow branches in Senegalia mellifera detinens
caused by the activity of termites (Kalotermitidae) [Fig.
5]. By eating the heartwood of dead branches and leaving
the outer wood and bark intact, the termites hollow out
branches, making small exit holes at the branching nodes.
This activity creates ideal daytime shelters for Afrogecko
ansorgii, with multiple entry and exit points. These
hollow branches subsequently break off and accumulate
below the tree, where they may still be used as refugia
by the geckos.
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Rediscovery of Afrogecko ansorgii in Angola
Table 1. Variation observed for Afrogecko ansorgii, comparing the type series from Maconjo, with new series obtained in Maconjo
and Sta Maria. Continuous measurements in mm (mean and range) for TL= total length, SVL= snout-vent length and Tail. Meristic
and qualitative variation (median and range) is given for number of precloacal pores and cloacal spurs.
TL SVL Tail Pores Spurs
Type Series — Maconjo
Females (n=2) 7) 45 30 0 na
New Series — Maconjo
Females (n=5)* Ts) 43.9 S03 0 ]
(71.4-79.0) (41.3-45.8) (30.1-33.2) 0 l
Males (n=4) 65 38.2 26.8 8 2
(57.8-68.8) (34.4—40.6) 23.4—29.0) 8-9 2
Juvenile Female (n=1) 68 38.6 29.4 0 1
New series — Sta Maria
Females (n=5)** 63.3 39.4 23.8 0 0
(56.2—69.3) (34.7—42.9) (22.0—26.4) 0) 0
Males (n=6)** 60 35.7 24.2
(53.2—63.5) (34.4-38.0) (18.8—27.5) fis 152
Juvenile Female (n=1) 54.4 B23 piers 0 0
* For Tail and TL measurements n=3 due to truncated tails; ** For Tail and TL measurements n=4 due to truncated tails.
Natural history: The geckos were mostly first seen lying
flat or moving slowly on thin branches in the early hours
of the evening. Nevertheless, they proved to be agile
when disturbed, often running along the branches or even
jumping between twigs. The tail was kept low most of
the time and appeared to be semi-prehensile. Based on
our observations they retreat to safety inside the hollow
branches of Senegalia mellifera detinens during the day,
and emerge soon after dark to forage, mostly on thin
branches but not restricted to the acacias. They likely
avoid the ground and no specimen was found walking
on soil or rock, but their agility allows them to move
across neighboring trees, particularly where there is a
high density of bushes, as at Maconjo, or where canopy
contact is facilitated by uneven and steep slopes as in Sta
Maria. A nocturnal arboreal foraging behavior has also
Fig. 3. Afrogecko ansorgii in its biotope, the termite-hollowed, thin branches of Senegalia mellifera detinens. ( )
hollow blackthorn twig. (B) Specimen caught trapped inside a blackthorn branch.
Amphib. Reptile Conserv.
been recorded for another Angolan endemic gecko, the
possibly closely related species Kolekanos plumicaudus,
although the latter retreats into rock crevices for shelter
(Agarwal et al. 2017).
The geckos probably prey on small insects found on
the outer branches of bushes, and it is possible that they
also feed on alates of the same termites that provide them
with the sheltering habitat, although this could not be
confirmed as gut content analyses were not performed.
The vast hollow branches with narrow entrances likely
preclude many snakes from preying on adults and eggs.
In any case, one specimen of Psammophis leopardinus
was collected, while actively moving at night among the
outer branches of a blackthorn bush at Maconjo (Fig.
6A), strongly suggesting that it was hunting A. ansorgii.
At both localities the gecko MHemidactylus cf.
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August 2019 | Volume 13 | Number 2 | e182
Vaz Pinto et al.
Fig. 4. Habitat of Afrogecko ansorgii. (A) Isolated granite outcrop beside the dry Cocumba stream near its confluence with Conjo
Stream (12°52’S, 13°21’E, 355 m asl), the correct site of Boulenger’s type locality “Maconjo’ for Phyllodactylus ansorgii and
Mabouia laevis. (B) Spiny savanna of Senegalia mellifera detinens with Terminalia prunioides and Aloe littoralis at the type
locality. (C) Scattered blackthorn bushes subject to thick morning fog and covered with lichen within which Afrogecko ansorgii was
rediscovered. (D) Aerial view of dry spiny savannah at the head of a valley leading down to Cape Sta Maria, Benguela Province
(13°31’S, 12°38’E, 288 m asl).
longicephalus was collected in syntopy in_ the
same bushes, although usually foraging on thicker
branches and closer to the ground. Other rupicolous
reptile species on the surrounding rocks on both sites
included Pachydactylus caraculicus, Chondrodactylus
fitzsimonsi, C. pullitzerae, Trachylepis laevis (Fig.
6B), 7) sulcata ansorgii, Agama planiceps, the diurnal
Rhoptropus cf. benguellensis and R. cf. barnardi; and the
terrestrial species Pachydactylus punctatus, Trachylepis
acutilabris, and Pedioplanis benguellensis. Species
found in Sta Maria but not recorded at Maconjo were
Afroedura cf. bogerti, Pachydactylus cf. oreophilus,
Cordylus namakuiyus, and Hemirhagerrhis viperina,
while Matobosaurus maltzahni, Agama anchietae,
Trachylepis binotata, and Psammophis leopardinus were
found at Maconjo but not at Sta Maria. These records
include northern extension ranges of roughly 200 km or
more for three gekkonids, Chondrodactylus fitzsimonsi,
Pachydactylus caraculicus, and Rhoptropus cf. barnardi,
and for the endemic and recently described Cordylus
namakuiyus (Stanley et al. 2016).
Distribution range: So far, the gecko has only been
found in the two referred localities of Maconjo and Cape
Sta Maria, spanning across over 100 km on Benguela’s
coastal plain. It is likely that the species has a wider
distribution range, where it may be locally common but
Amphib. Reptile Conserv.
irregularly distributed, and dependent on very particular
habitat requirements in association with Senegalia
mellifera detinens and the kalotermitid termites.
New series and morphological variation: The new
material obtained in both localities is consistent with
the original description of Afrogecko ansorgii. The more
slender form and the enlarged precloacal scales well
distinguish this species from A. porphyreus (Daudin
1802), while the larger size, presence of femoral spurs
and a slender semi-prehensile versus a broad flattened
tail clearly separates it from the other Angolan endemic
Leaf-toed Gecko Kolekanos plumicaudus (Haacke 2008).
Boulenger’s description, based on one of two available
adult females, is terse but conforms to that of the era and
is given below, while some measurements, including the
new series, are presented in Table 1. Male specimens
were obtained for the first time, allowing comparisons
between sexes and localities. A detailed re-description
of A. ansorgii is being prepared, which will also explore
phylogenetic relationships and include a taxonomic
review (data not shown). Original description of
Afrogecko ansorgii (Boulenger 1907):
Head rather small, oviform, much longer than broad;
snout not longer than the distance between the eye
and the ear opening, which is small and oval. Body
August 2019 | Volume 13 | Number 2 | e182
Rediscovery of Afrogecko ansorgii in Angola
ti vie
K..
aa
poe
we
Fig. 5. Kalotermitid termites active on blackthorn bushes at type locality. (A) Hollow branch in tree. (B) Termite soldier and
evidence of wood excavation. (C) Termite and eggs inside branch. (D) Workers active inside hollow branch.
very elongate; limbs moderate. Digits moderately
depressed, with large, subtrapezoid terminal
expansions; eight lamellae under the fourth toe. Head
and body covered with uniform, smooth, flattened
granules, which are larger on the snout and on the
belly. Rostral twice as broad as deep, without cleft
above; symphysial small, a little longer than broad;
ten upper and as many lower labials,; rostral and first
upper labial entering the nostril; no chin-shields. Tail
cylindrical, tapering, covered with uniform, small,
quadrangular, smooth scales. A curved transverse
series of eight or nine enlarged praeanal scales
(indicating praeanal pores in the male?). Pale greyish
brown above, with a series of large whitish spots along
each side of the back; a dark streak on each side of the
head and neck, passing through the eye; upper lip and
lower parts white, with small brown spots.
Two females collected in the type locality were gravid
with two eggs (Fig. 7A). Male specimens are noticeably
smaller than females in snout-vent and total length, with
the difference being more pronounced at the type locality.
As predicted by Boulenger, males have 7—9 precloacal
pores (Fig. 7B), corresponding to the enlarged scales
found on females (Fig. 7C). Of note are the differences
found between the series obtained at Maconjo and
Sta Maria. Specimens from Maconjo proved to be
consistently larger in size and overall measurements,
Amphib. Reptile Conserv.
with females from Sta. Maria of approximately similar
size as males from Maconjo (Table 1). Also striking is the
presence of more cloacal spurs in the series from the type
locality. Although not mentioned in the type description,
we found one cloacal spur in females from Maconjo (Fig.
7A), and two spurs in males from same locality (Fig. 7B).
On the other hand, females from Sta Maria showed no
cloacal spurs, while at the same site all males but one had
one single spur (Table 1).
Discussion
The traditional reliance of gekkonid systematics on
digital morphology is often reflected in the generic
names, with the Leaf-toed Geckos, Phyllodactylus
being one of numerous examples. Until the end of the
20" century, gecko species assigned to Phyllodactylus
had a patchy distribution, spread across five continents.
Increasing awareness of both the antiquity of gekkotan
lineages (Kluge 1987; Conrad and Norell 2007), of
the taxonomic confusion generated by their conflicting
conservative and sometimes convergent morphologies
(Bauer et al. 1997; Gamble et al. 2012), and of the
development and application of molecular phylogenetic
studies (Han et al. 2004; Wiens et al. 2012), have resulted
in a true understanding of gecko antiquity and diversity.
Taxonomic re-arrangements to reflect this evolution and
August 2019 | Volume 13 | Number 2 | e182
Vaz Pinto et al.
x
er
i . oo
om 2 we:
a ae a
ee
ve Se et hea,
Fig. 6. (A) Specinieh of Psammophis leopardinus Bimeine at neHe ona blackthorh Bish at Eyal TARE — on A A.
ansorgii. (B) First topotypic material of TZrachylepis laevis collected in over 110 years, FKH0018 in life; note flattened body adapted
to shelter among tight rocky spaces.
cryptic diversity has resulted in the genus Phyllodactylus,
as understood for over 100 years, now being distributed
among the families Diplodactylidae, Gekkonidae, and
Phyllodactylidae and in at least 15 genera! It is thus
not surprising that the generic affinities of Afrogecko
ansorgii remain problematic. When initiating a major
generic revision of phyllodactyline geckos, Bauer et al.
(1997) provisionally assigned ansorgii (then known only
from the types) to the genus Afrogecko, but noted that its
affinities would need re-assessment on discovery of new
material.
Subsequently Haacke (2008) described the new plume-
tailed gecko from the Angolan Namib region that was
again tentatively assigned as Afrogecko plumicaudus in
the absence of genetic studies. The collection of additional
new material by Wulf Haacke allowed its phylogenetic
affinities to be assessed, whereupon it was transferred to
anew gekkonine genus Kolekanos (Heinicke et al. 2014).
Although all the original material was collected under
thin, exfoliating rock slabs, the species was later shown
to forage arboreally (Agarwal et al. 2017). In its (at least)
partial arboreal behavior, K. plumicaudus is similar to
A. ansorgii. Nevertheless, A. ansorgii 1s unique among
southern African leaf-toed geckos, in being exclusively
arboreal and by what appear to be some remarkable
ecological adaptations. The morphological differences
found in specimens obtained at the type locality and Sta
Maria, namely in body size and number of cloacal spurs,
likely reflect local adaptations and may be climatically
driven. Further detailed morphological and genetic
studies are ongoing to confirm the generic placement of
A. ansorgii and explore intraspecific variation (data not
shown).
Southwestern coastal Angola is subject to frequent
advective fogs and relatively cool temperatures, caused
by the cold offshore Benguela current, and experiences
a climatic gradient of increased rainfall from the coast
inland (Huntley 2019). The importance of advective fog
and low clouds in shaping the local arid ecosystems has
been relatively well studied in Namibia, where it has
been estimated to represent up to five times the amount
of precipitation provided by rain (Seeley and Henschel
1998). The frequency of this type of fog is high in coastal
areas, but studies in the central Namib found the amount
of precipitation to be highest around 35—60 km inland
and below 500 m asl, where low strata clouds were
Amphib. Reptile Conserv.
37
intercepted by local elevation (Lancaster 1984). Satellite
imagery show that advective fog and low clouds penetrate
further inland in the southern and northern sections of
the Namib (Cermak 2012), but relatively little effort has
focused on the role of fog and low clouds in Angola.
Nevertheless, it has been suggested that the incidence of
winter fog and low strata clouds is especially pronounced
between the towns of Namibe and Benguela, leading to
heavy morning dew and allowing for a local abundance
of epiphytic lichens (Huntley 2019). The presence of
these epiphytic lichens was recorded at the site of Sta
Maria, where they often almost covered the branches
of blackthorn bushes. Being close to the sea shore and
situated in an extensive dry valley, the collecting site
at Sta Maria is subject to frequent morning coastal
Fig. 7. (A) Female Afrogecko ansorgii from Maconjo,
FKH0007, gravid with two eggs. Note enlarged precloacal
scales and presence of one cloacal spur. (B) Cloacal region
of male A. ansorgii, FKHO008. Note single chevron row of
nine precloacal pores, hemipenial bulges (as paired light
swellings) and cloacal spurs (small white tubercular scales on
lateral surfaces of tail base) in the male. (C) Cloacal region of
female A. ansorgii, FKH0009. Note lack of precloacal pores on
the chevron row of enlarged scales or of enlarged tubercular
lateral scales on tail base. Both sexes have delicate elongate
toes with a single pair of terminal scansors. The cylindrical tail
is finely scaled, and non-verticillate, lacking obvious lateral
constrictions.
August 2019 | Volume 13 | Number 2 | e182
Rediscovery of Afrogecko ansorgii in Angola
advective fogs which become trapped among high rocky
slopes. Although lichens were less abundant at Maconjo,
the type locality also appeared to be regularly subject
to thick foggy conditions. Situated at around 40 km
from the coast and 400 m asl, Maconjo lies at the base
of a north-south oriented orographic step, characterized
by mountainous granitic hills that elevate the coastal
plateau further east to above 800 m asl, and therefore
topography likely plays a role in containing fog and
low strata clouds and, ultimately, shaping the ecological
conditions of local spiny savannas. The blackthorn bush
holds a reputation for being termite-resistant (Schmidt et
al. 2002). Nevertheless, in both Maconjo and Sta Maria
we found ‘drywood’ termites (family Kalotermitidae) to
be present inside dead blackthorn branches, often leaving
them neatly excavated. This was especially evident at the
drier environment of Sta Maria, where large numbers
of dead branches break and accumulate on the ground
underneath the bush canopy, thus providing an abundance
of sheltering habitat for the gecko. Drywood termites are
well adapted to arid ecosystems but may also require
some moisture and tend to be uncommon or patchily
distributed. It appears therefore that the local distribution
of termites is driven by specific environmental conditions
affecting the bushes of Senegalia mellifera detinens, like
altitude and rainfall, atmospheric moisture provided
by fog or low clouds, and the frequency and severity
of droughts. In regions with relatively higher moisture
from average rainfall, these blackthorn savannas may not
accumulate enough dead wood and the conditions might
be unsuitable for the termites and ultimately the gecko.
On the other hand, under extremely dry conditions the
termites may not thrive, or the density of bushes might be
too low, not providing enough shelter or foraging habitat
for this exclusively arboreal gecko. Therefore, the dry
coastal blackthorn savannas that experience low rainfall
but are subject to frequent fogs, seem to constitute the
‘sweet spot’ habitat for the species.
Formerly known locally as Deserto de Mossamedes,
the northernmost extension of the Namib Desert stretches
north along the Atlantic coast of Angola from the Angola-
Namibia border for 450 km to about the city of Benguela.
Fronting the Atlantic Ocean to the west, it gradually
ascends in elevation eastward to a semiarid plain
dominated by acacia and mopane [African ironwood]
trees that abuts the steep Serra de Chela escarpment.
Characterized by gravel plains and rock platforms
interspersed with sand dune fields, the Angolan Namib
is part of a broader ecoregion defined as Kaokoveld
Desert (Burgess 2004). It is believed that ancient climatic
stability, a mosaic of substrates and incidence of coastal
fogs contribute to high species richness and rates of
endemism in the Namib region (Seeley et al. 1998), and
the Kaokoveld is often referred to as a regional center
of endemism for flora (Van Wyk and Smith 2011),
beetles (Koch 1961), and lizards (Lewin et al. 2016;
Branch et al. 2019b). Nevertheless, the boundaries of the
northern Kaokoveld have remained poorly defined and
although Burgess (2004) depicted the ecoregion along
the Angolan coast to about Benguela town, other authors
have set the northern limit at Lucira, in Namibe Province
(e.g., Craven 2009; Branch et al. 2019). Between Lucira
Amphib. Reptile Conserv.
and Benguela the semi-arid ecosystems characterized by
a diversity of succulent plants progressively gives way
to semi-arid dry savannas dominated by acacia species
(Barbosa 1970), thus placing our surveyed sites on the
fringes of the Kaokoveld ecoregion. Historical and recent
herpetological work on the Angolan arid ecosystems
has mostly focused in the southernmost regions of the
Angolan Kaokoveld (Marques et al. 2018; Branch
et al. 2019b), and about one-third of national reptile
diversity is known to occur in the Namibe Province
alone, with gekkonids being the most speciose group
(Ceriaco et al. 2016). In comparison, less effort has
been directed to Benguela Province, yet the diversity
and new extension ranges here reported suggest that
the herpetological richness of the province may have
been underestimated. It is likely that future surveys
across the northern limits of the Kaokoveld will further
increase the regional lists, unveil cryptic diversity, and
underline the ecological significance of the local spiny
semi-arid savannas associated with fog and low strata
clouds. Apparently restricted to Benguela’s Kaokoveld
and strongly associated with the local fog ecosystem,
the now rediscovered Ansorge’s gecko remains as one of
the most unique and iconic representatives of Angolan
herpetofauna.
Acknowledgements.—We thank our various companions
for their help and camaraderie, both 1n the field and in
general: Ninda Baptista, Afonso Vaz Pinto, Kostadin
Luchansky, and Werner Conradie. Scientific collaboration
is enriched by such synergy and stimulation. In addition,
we thank the National Geographic Okavango Wilderness
Project (National Geographic Society grant number
EC0715-15) for funding fieldwork and biodiversity
surveys in Angola, and the Ministry of Environment
(MINAMB) for issuing research and export permits. We
thank Wulf Haacke for discussion on his early exploration
of Angola in the 1970s, when he made numerous
discoveries, many still unpublished. We are also indebted
to Fernanda Lages and to ISCED — Jnstituto Superior de
Ciéncias da Educagao da Huila for logistical support.
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Vaz Pinto et al.
Pedro Vaz Pinto is Angolan and was born 1n Luanda, Angola in 1967. Pedro graduated
in Forest Engineering at Technical University of Lisbon, and obtained a doctoral
degree in Biology from the University of Porto, Portugal. Over the past 20 years,
he has worked in biodiversity conservation in Angola addressing rare or endangered
species, and protected area management. Pedro is a director for the local NGO Kissama
Foundation, and a researcher for CIBIO-InBio. His studies on Angolan vertebrates
have focused mostly on genetics, biogeography, and conservation in antelopes, birds,
reptiles, and amphibians. Pedro travels the country extensively and has received three
international environmental awards for his biodiversity conservation work in Angola.
Luis Verissimo is Portuguese and was born in Lisbon, Portugal, in 1971. He graduated
in Geography from the University of Lisbon, and obtained a Master’s degree in Applied
Ecology from the Michigan Technological University in the United States. Luis is a
geospatial specialist and ecologist with 20 years of experience conducting geospatial
data analysis, cartography, and field and survey investigations for land-based,
freshwater, and marine applications. He has worked extensively on the vertebrates of
Angola addressing biogeography, conservation, and historical distribution. Luis has
also been actively engaged in the assessment of existing and establishment of new
protected areas within Angola’s framework of national parks and reserves.
Bill Branch (William R. Branch) was born in London, United Kingdom. He was employed as Curator of Herpetology at
the Port Elizabeth Museum for over 30 years (1979-2011), and upon his retirement he was appointed Curator Emeritus
Herpetology until his death in October 2018. Bill’s herpetological studies concentrated mainly on the systematics,
phylogenetic relationships, and conservation of African reptiles, but he has been involved in numerous other studies on
the reproduction and diet of African snakes. He has published over 300 scientific articles, as well as numerous popular
articles and books. The latter include: South African Red Data Book of Reptiles and Amphibians (1988), Dangerous
Snakes of Africa (1995, with Steve Spawls), Field Guide to the Reptiles of Southern Africa (1998), Tortoises, Terrapins
and Turtles of Africa (2008), and Atlas and Red Data Book of the Reptiles of South Africa, Lesotho and Swaziland
(multi-authored, 2014), as well as smaller photographic guides. In 2004, he was the 4" recipient of the “Exceptional
Contribution to Herpetology” award of the Herpetological Association of Africa. Bill has undertaken field work in over
16 African countries, and described nearly 50 species, including geckos, lacertids, chameleons, cordylids, tortoises,
adders, and frogs.
Amphib. Reptile Conserv.
41 August 2019 | Volume 13 | Number 2 | e182
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 42—56 (e184).
€ptile-cons™
Phylogeography of the East African Serrated Hinged Terrapin
Pelusios sinuatus (Smith, 1838) and resurrection
of Sternothaerus bottegi Boulenger, 1895 as a subspecies
of P. sinuatus
‘Melita Vamberger, 7Margaretha D. Hofmeyr, *Courtney A. Cook,
45Edward C. Netherlands, and °*Uwe Fritz
‘6 Museum of Zoology, Senckenberg Natural History Collections Dresden, A. B. Meyer Building, 01109 Dresden, GERMANY ?Chelonian Biodiversity
and Conservation, Department of Biodiversity and Conservation Biology, University of the Western Cape, Bellville 7535, SOUTH AFRICA ?4Unit
for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom 2520, SOUTH AFRICA *Laboratory of
Aquatic Ecology, Evolution and Conservation, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven, BELGIUM
Abstract.—Pelusios sinuatus is distributed in East Africa from southern Ethiopia and Somalia to northeastern
South Africa. Inland it reaches westernmost Zimbabwe, Rwanda, and Burundi. Despite this wide range, which
spans in north-south direction across 3,500 km and in east-west direction more than 1,500 km, no geographic
variation has been described. However, using phylogenetic and haplotype network analyses of mitochondrial
and nuclear DNA (2,180 bp and 2,132 bp, respectively), phylogeographic variation is herein described, with two
distinct genealogical lineages. One occurs in the northern and central parts of the distribution range, and the
other is in the south. Terrapins representing the southern lineage attain a smaller maximum body size than
terrapins from the northern and central parts of the range. The distribution ranges of the two lineages abut
in the border region of Botswana, South Africa, and Zimbabwe. We conclude that each lineage represents a
distinct subspecies, with the nominotypical subspecies Pelusios sinuatus sinuatus (Smith, 1838) occurring in
the south and the newly recognized subspecies Pelusios sinuatus bottegi (Boulenger, 1895) in the central and
northern distribution range. We found phylogeographic structuring within each subspecies and propose that
the differentiated population clusters should be recognized as Management Units.
Keywords. management units, Pelomedusidae, systematics, taxonomy, Testudines, turtle
Citation: Vamberger M, Hofmeyr MD, Cook CA, Netherlands EC, Fritz U. 2019. Phylogeography of the East African Serrated Hinged Terrapin
Pelusios sinuatus (Smith, 1838) and resurrection of Sternothaerus bottegi Boulenger, 1895 as a subspecies of P. sinuatus. Amphibian & Reptile
Conservation 13(2): [Special Section]: 42-56 (e184).
Copyright: © 2019 Vamberger et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 6 February 2019; Accepted: 5 June 2019; Published: 19 August 2019
Introduction Pelomedusids and podocnemidids are both of Gondwanan
origin (de Broin 1988; Noonan 2000) and, together with
The freshwater turtle genus Pe/usios comprises 17 — the Australasian and South American family Chelidae,
species distributed across sub-Saharan Africa, with — represent the chelonian suborder Pleurodira (side-necked
most likely introduced populations on Madagascar, the turtles; TTWG 2017).
Seychelles, and Guadeloupe in the Lesser Antilles (Fritz In addition to a number of species with localized
et al. 2011, 2013; Stuckas et al. 2013; TTWG 2017). All narrow distribution, Pe/usios also includes species
species of Pe/usios are side-necked turtles characterized — with wide distributions (Branch 2008; TTWG 2017).
by a plastral hinge that allows partial or complete closure The Serrated Hinged Terrapin, P sinuatus (Smith,
of the anterior shell opening (Bramble and Hutchison 1838), has one of the largest distribution ranges of all
1981; Branch 2008). Together, Pe/usios and its African- — Pe/usios species. It occurs in East Africa from southern
Arabian sister genus Pelomedusa, which has 10 formally — Ethiopia and Somalia southwards to Eswatini (formerly
recognized species (Petzold et al. 2014; TTWG 2017), Swaziland) and northeastern South Africa (Branch 2008;
constitute the family Pelomedusidae that is sister to ©TTWG 2017; Fig. 1). The Serrated Hinged Terrapin has
the New World-Madagascan family Podocnemididae. _ the largest body size in its genus and may reach up to
Correspondence. * wwe.fritz@senckenberg.de
Amphib. Reptile Conserv. 42 August 2019 | Volume 13 | Number 2 | e184
Vamberger et al.
Botswana
Mozambique A3
Botswana
South Africa
(Limpopo, B1
Mpumalanga)
Pelusios sinuatus 1.0
Mozambique
Zimbabwe
South Africa
(KwaZulu-Natal, B2
Limpopo)
Pelusios marani
0.4
Fig. 1. Left: Sampling sites and mitochondrial identity of Pe/usios sinuatus used in the present study. Divided symbols indicate
syntopic occurrences of the respective subclades. Terrapin shapes symbolize differences in maximum sizes of the northern and southern
P. sinuatus (see Discussion section). Inset: Distribution range of P. sinuatus according to the TTWG (2017) with the type localities
of taxa referred to this species. (1) Sternothaerus bottegi Boulenger, 1895: Bardere (Bardera), Somalia; (2) Pelusios sinuatus leptus
Hewitt, 1933: Isoka, Zambia; (3) Sternotherus sinuatus Smith, 1838 — restricted type locality (Broadley, 1981): confluence of Crocodile
and Marico Rivers, Limpopo (Transvaal); (4) Pe/usios sinuatus zuluensis Hewitt, 1927: Mzinene River (Umsinene River, Zululand),
KwaZulu-Natal. Right: Bayesian tree for 61 Pe/usios sinuatus using 2,180 bp of mitochondrial DNA. Clades are collapsed to cartoons
showing the deepest genetic divergence within each clade. Outgroup Pelomedusa variabilis was removed for clarity. Numbers above
the nodes are posterior probabilities; below the nodes, thorough bootstrap values under ML. Full trees are available from https://
figshare.com/s/52a7af23cff3aa08ea75. Inset: Adult Pelusios sinuatus, Bonamanzi, KwaZulu-Natal, South Africa.
55 cm in shell length (Spawls et al. 2002). In contrast a distribution range similar to that of P sinuatus, was
to other Pelusios species, P. sinuatus is a deep-water — characterized by moderate phylogeographic variation
terrapin that occurs in perennial rivers, lakes, and larger _— (Fritz et al. 2013).
man-made water bodies in savannah regions. During the Until now, neither the morphological nor the
rainy season, Serrated Hinged Terrapins move overland, phylogeographic variation of P sinuatus has been
and they colonize smaller water bodies, like pans and studied systematically. The species has traditionally
waterholes (Broadley and Boycott 2009). In eight other been regarded as monotypic (Ernst and Barbour 1989;
widespread Pelusios species, Fritz et al. (2013) and TTWG 2017; Wermuth and Mertens 1961, 1977),
Kindler et al. (2016) found that phylogeographic patterns = even though Hewitt (1927, 1933) had described two
were not correlated with habitat type, with some species — subspecies from South Africa and Zambia that were
displaying pronounced phylogeographic structuring soon synonymized (Loveridge 1936). However, using
and others not. Among the studied savannah species, P. mitochondrial and nuclear DNA sequences of only two
rhodesianus showed a deep phylogeographic structure samples from KwaZulu-Natal (South Africa) and another
and could actually represent a species complex (Kindler — one from Botswana, Fritz et al. (2011) found two genetic
et al. 2016), whereas phylogeographic structuring in lineages, suggesting that an in-depth investigation of
P. nanus and P. subniger was negligible. However, the — genetic variation may reveal further differentiation.
westernmost studied population originally identified as § The present paper presents the first assessment of the
P. subniger (in Democratic Republic of the Congo) was genetic variation of P sinuatus across its range. The
found to represent a genetically distinct undescribed results are discussed with respect to taxonomy and two
species. Unfortunately, samples from the northern — subspecies are recognized within P. sinuatus. To this end,
distribution area of P. subniger were not available for | Sternothaerus bottegi Boulenger, 1895 is resurrected
study, so nothing is known about the genetic identity of | from the synonymy of P. sinuatus (Smith, 1838), in
the northern populations (Fritz et al. 2013; Kindler et al. | which it was placed soon after its description (Calabresi
2016). Another savannah species (P. castanoides), with 1916; Siebenrock 1916).
Amphib. Reptile Conserv. 43 August 2019 | Volume 13 | Number 2 | e184
Phylogeography of Pelusios sinuatus in East Africa
Materials and Methods
Sampling, chosen loci, and general data evaluation
strategy: Sixty-one samples of Pe/usios sinuatus from
Botswana, Mozambique, South Africa, and Tanzania
were studied, including previously published data for
three terrapins (Appendix 1). The same mitochondrial
and nuclear DNA fragments were targeted as in earlier
studies on Pelusios (Fritz et al. 2011; Kindler et al. 2016).
Three mitochondrial DNA fragments were sequenced
(12S, cyt 6, and ND4 with adjacent DNA coding for
tRNAs). In addition, two protein-coding nuclear genes
(Cmos and Rag2) and intron 1 of the nuclear R35 gene
were sequenced. Details of DNA isolation, PCR, and
sequencing are described in Kindler et al. (2016). The
12S sequences obtained were up to 398 bp long (with
gaps); the cyt b sequences were up to 913 bp; and the
mtDNA sequences comprising the partial ND4 gene
plus adjacent DNA coding for tRNAs were up to 869
bp long. All nuclear DNA blocks could be sequenced
directly. Cmos sequences had lengths of up to 358 bp;
R35 sequences, up to 1,101 bp; and Rag2 sequences,
up to 673 bp. Sequences were aligned and inspected
using BioEdit 7.0.5.2 (Hall 1999). All sequences aligned
perfectly and gaps occurred only in sequence blocks not
coding for proteins.
Mitochondrial DNA is maternally inherited, whereas
nuclear loci are inherited biparentally. Moreover,
mtDNA is prone to introgression, including across
species borders, which often leads to conflicting results
for the two marker systems (Currat et al. 2009; Funk and
Omland 2003; Kehlmaier et al. 2019; Sloan et al. 2017;
Toews and Brelsford 2012). To avoid the risk of such
distortion, mitochondrial and nuclear sequence data were
examined separately.
Phylogenetic analyses: Individual mtDNA fragments
were concatenated for phylogenetic analyses, and this data
set was combined with previously published sequences,
resulting in an alignment of 2,180 bp length. The dataset
included 61 sequences of Pelusios sinuatus and, as
outgroups, one sequence each of Pelomedusa variabilis
and Pelusios marani. European Nucleotide Archive
(ENA) accession numbers and collection sites are given in
Appendix |. The best partitioning scheme was determined
using PartitionFinder (Lanfear et al. 2012) and the
Bayesian Information Criterion (BIC). Three partitioning
schemes were tested: (1) unpartitioned, (2) partitioned by
mtDNA fragment, and (3) partitioned by gene and codon
position with DNA not coding for proteins (1.¢e., 12S and
DNA coding for tRNAs) corresponding to one additional
partition each. According to the results of PartitionFinder,
scheme (3) was selected.
Phylogenetic relationships were inferred using
Bayesian and Maximum Likelihood (ML) approaches.
Bayesian trees were obtained with MrBayes 3.2.6
(Ronquist et al. 2012) using the partitioning scheme
and evolutionary models shown in Table 1 and default
parameters. Two parallel runs, each with four chains, were
conducted. The chains ran for 10 million generations,
with every 500" generation sampled. The calculation
parameters were analyzed using a burn-in of 2.5
Amphib. Reptile Conserv.
44
million generations to assure that both runs converged.
Subsequently, only the plateau of the remaining trees
was sampled using the same burn-in, and a 50% majority
rule consensus tree was generated. Tracer 1.7 (Rambaut
et al. 2018) served to check for convergence of the runs
using the Effective Sample Sizes (ESS) of parameters,
and resulted in ESSs over 200 after discarding the burn-
in. In addition, phylogenetic relationships were inferred
under ML using RAxML 7.2.8 (Stamatakis 2006) and
the GTR+G substitution model across all partitions. Five
independent ML searches were performed using different
starting conditions and the fast bootstrap algorithm
to explore the robustness of the results by comparing
the best trees. Then, 1,000 non-parametric thorough
bootstrap replicates were calculated and the values were
plotted against the best tree.
Parsimony networks: For each mitochondrial and
nuclear DNA fragment, a parsimony network was
constructed using Popart (http://popart.otago.ac.nz).
Since the underlying TCS algorithm is sensitive to
missing data, a few individuals represented by short
sequences were excluded. In addition, for achieving
complete coverage, the lengths of mtDNA sequences
were trimmed, resulting in an alignment of 348 bp length
for 12S, 784 bp for cyt 5, and 737 bp for ND4 + DNA
coding for tRNA. For network construction of nuclear
data, heterozygous sequences of R35 were phased
using the Phase algorithm in DnaSP 5.10 (Librado and
Rozas 2009), and two identical copies for homozygous
sequences of all loci were included. Nuclear DNA
sequences for the networks had the same lengths as given
above.
Uncorrected p distances and isolation by distance for
mtDNA: Uncorrected p distances were calculated for the
mitochondrial cyt b gene alone as well as for the mtDNA
alignment of concatenated sequences using MEGA
7.0.21 (Kumar et al. 2016) and the pairwise deletion
option. The distances of the concatenated sequence data
were used to examine for a positive correlation between
geographic and genetic distances (isolation by distance).
For this purpose, Mantel tests as implemented in IBD
1.52 (Bohonak 2002) were run for three data sets using
genetic and spatial distances. The latter were obtained via
the Geographic Distance Matrix Generator 1.2.3 (http://
biodiversityinformatics.amnh.org/open_source/gdmg/
index.php). The significance of the slope of the reduced
major axis (RMA) regression was assessed by 30,000
randomizations. One data set included the sequences
for all 61 terrapins. The other two data sets included the
sequences for each clade of P. sinuatus (clades A and B)
identified in the present study.
Table 1. Partitioning and evolutionary models used for
MrBayes.
Subset nst rates Model
1-398 401-1311\3 1314- 6 gamma SYM+ gamma
1998\3 1999-2180
399-1311\3 1312-1998\3 6 SYM
400-1311\3 1313-1998\3 6 gamma SYM+ gamma
August 2019 | Volume 13 | Number 2 | e184
Vamberger et al.
Body size: Using Vernier calipers (accuracy 0.1 mm),
straight carapace length of adult terrapins was recorded as
a measure of body size during fieldwork in South Africa
(n = 11). Also measured were specimens in the Museum
for Comparative Zoology, Cambridge, Massachusetts,
USA (MCZ 39383, South Africa), the Museum fir
Naturkunde, Berlin, Germany (ZMB 158, Mozambique;
ZMB 5517, 5518, 15689, 16158, 16242, Tanzania; ZMB
22416, Burundi), the Museum fiir Tierkunde (Museum
of Zoology), Senckenberg, Dresden, Germany (MTD D
49650, South Africa), and the Palaontologisches Institut
und Museum, Zurich, Switzerland (PIMUZ A/III527,
Tanzania). Measurements were divided into northern
and southern groups according to the two genetic clades
identified in the present study. Since males and females
could not be distinguished in all samples, the two sexes
were combined for analysis. After testing for whether the
data were parametric, the body sizes of the groups were
compared using a f-test as implemented in SigmaPlot
13.0 (Systat Software, Inc., San Jose, California, USA).
Results
Phylogenetic and haplotype network analyses of
mtDNA: Both tree-building approaches delivered the
same topology, corresponding to two geographically
widespread clades, A and B, both of which showed
substructuring and received high support values (Fig.
1). Clade A corresponded to the samples from the north
and center of the distribution range of Pe/usios sinuatus
(Tanzania, Mozambique, and Botswana), and clade B to
samples from the south (Botswana and South Africa).
Clade A consisted of three subclades and clade B, of
two. All subclades of clade A and one subclade of clade
B were well supported under both Bayesian and ML
analyses; the second subclade of clade B was moderately
supported. In Botswana and northeastern South Africa,
records of terrapins representing clades A and B are only
separated by a distance of approximately 200 km, and in
northeastern South Africa, representatives of subclades
B1 and B2 were found in two sites syntopically.
In haplotype networks of the three mtDNA fragments,
no shared haplotypes occurred for the two clades (Fig. 2).
Four 12S haplotypes were found for clade A, with two
private haplotypes for subclade A2 that differed by one
mutation step each from a shared haplotype that included
sequences of subclades Al and A3. Another private
haplotype of subclade A3 also differed by one mutation
step from the previously mentioned shared haplotype.
This shared haplotype was separated by three mutation
steps from a common haplotype containing sequences
of subclades B1 and B2, and a second rare haplotype
for subclade B1 differed by one mutation step from this
common haplotype. Haplotype networks of the two other
mtDNA fragments showed more differentiation, with
no shared haplotypes between any clades or subclades.
For the cyt 5 fragment, haplotypes of clades A and
B were separated by a minimum of 21 steps. Within
haplotypes of clade A, up to 10 mutations occurred, with
each subclade corresponding to one distinct haplotype.
Within haplotypes of clade B, a loop occurred that
connected three of the four haplotypes of subclade B1;
Amphib. Reptile Conserv.
45
and the four haplotypes of this subclade were separated
by a minimum of four steps from the three haplotypes
of subclade B2, each of which differed by one mutation
step. With respect to the mtDNA fragment containing the
partial ND4 gene and adjacent DNA coding for tRNAs,
haplotypes of clades A and B differed by a minimum
of 13 mutations. Subclade Al was represented by one
haplotype. Subclade A2 consisted of three haplotypes
that each differed by a maximum of three mutations; and
subclade A3 had four haplotypes that differed by up to
four steps. Within the individual haplotypes of clade A, a
maximum of nine steps occurred, and the three subclades
were separated by a minimum of 4—7 steps. The three
haplotypes of subclade B1 differed by a maximum of
two mutations and the two haplotypes of subclade B2,
by one mutation, and the two subclades were distinct by
a minimum of six steps.
Haplotype network analyses of nuclear loci: The three
nuclear loci showed distinctly less variation compared to
the mtDNA fragments. Often, shared haplotypes between
distinct clades and subclades were found (Fig. 3). For
the Cmos gene, the 15 haplotypes found differed by a
maximum of nine mutation steps. Clades A and B shared
two haplotypes, even though the vast majority of phased
sequences of clades A and B corresponded to unique
haplotypes for each clade. A generally similar picture was
revealed for the Rag2 locus, with one shared haplotype of
clade A and clade B, six unique additional haplotypes of
clade A, and three further unique haplotypes of clade B.
The maximum number of mutations between the Rag2
haplotypes was seven. For intron 1 of the R35 gene, no
shared haplotypes were found for clades A and B. A total of
15 haplotypes occurred that were partially connected over
a loop. In a direct line (not across the loop), the haplotypes
differed by up to seven mutations. Of the 15 haplotypes,
six corresponded to clade A and nine to clade B.
Uncorrected p distances and isolation by distance for
mtDNA: Sequence divergences of the mitochondrial cyt
b gene are often used to distinguish between chelonian
taxa (e.g., Iverson et al. 2013; Kindler et al. 2012,
2016; Petzold et al. 2014). The uncorrected p distance
between clade A and clade B of P. sinuatus amounted to
2.80% on average, while the within-group values were
1.05% and 0.28%, respectively. Between the individual
subclades of clade A, divergences ranged between 1.31%
and 1.54%, with no variation within those two clades
for which sequences of more than one individual were
available. Subclades B1 and B2 differed by only 0.57%,
with within-group divergences of 0.06% and 0.02%,
respectively (Table 2).
The IBD test for all data revealed a statistically
significant correlation of genetic and geographic distances
(Z = 22487528, r = 0.65, p < 0.0001; n = 61). When
the two clades were analyzed separately, a statistically
significant correlation was also found for clade A (Z =
1387859, r= 0.58, p < 0.0003; n= 17), but not for clade
B (Z = 9009469796357, r = 0.06, p < 0.0777; n= 44).
Body size: The mean straight carapace length (+ SD)
for the samples of the northern and southern clades,
August 2019 | Volume 13 | Number 2 | e184
Phylogeography of Pe/usios sinuatus in East Africa
ies @ ai
3 12S a es @ A2
n=60 7 » © A3
©) B1
18 2
cyt b
n=48 3
ND4+tRNAs
n=61
Fig. 2. Parsimony networks for individual mtDNA fragments of Pelusios sinuatus. Symbol size is proportional to haplotype
frequency. Each line connecting two haplotypes corresponds to one mutation step, if not otherwise indicated by numbers of
substitutions along the lines. Colors correspond to Fig. 1. Small black circles represent missing node haplotypes.
n=106 ac
Fig. 3. Parsimony networks for nuclear loci of Pe/usios sinuatus. Symbol size is proportional to haplotype frequency. Each line
connecting two haplotypes corresponds to one mutation step, if not otherwise indicated by numbers of substitutions along the lines.
Colors correspond to Fig. 1. The small black circle represents a missing node haplotype. Sample sizes refer to phased nuclear
sequences, i.e., each individual is represented twice.
Amphib. Reptile Conserv. 46 August 2019 | Volume 13 | Number 2 | e184
Vamberger et al.
HB North n=7
South n=14
Individuals
2
| | } I
0 -
30 35 40 45
a 10 15 20 25
Carapace length (straight line, cm)
Fig. 4. Carapace lengths of adult Pel/usios sinuatus from
the northern and the southern distribution range (museum
specimens and wild-caught terrapins), corresponding to clades
A (north) and B (south).
respectively, were 31.8 + 7.9 cm (n= 7) and 24.0 + 5.5
cm (n= 14), with terrapins from the northern clade being
significantly larger than those from the southern clade (t,,
= 2.66, p = 0.0156).
Discussion
The present study is the first assessment of the
phylogeography for the Serrated Hinged Terrapin
(Pelusios sinuatus), which is widely distributed in
East Africa (TTWG 2017; inset in Fig. 1). In north-
south direction, the distribution area extends over
approximately 3,500 km and in east-west direction,
over more than 1,500 km. Within this large area,
two mitochondrial clades (A and B) with parapatric
distribution and substantial geographic substructure were
discovered (Figs. 1 and 2). In contrast to mitochondrial
DNA, the slower evolving nuclear DNA has not reached
complete lineage sorting for the Cmos and Rag2 loci
(Fig. 3), even though haplotype sharing between clades
A and B was restricted. For intron 1 of the R35 gene,
no shared haplotypes occurred. Thus, mitochondrial and
nuclear markers show largely concordant differentiation
patterns.
Clade A was found in the northern and central parts
of the distribution range (Tanzania, Mozambique, and
Botswana), and clade B, in the south (Botswana and
South Africa). Close to the border region of Botswana,
Zimbabwe, and South Africa the two clades abut, which
explains why Fritz et al. (2011) had already discovered
the two clades using only three samples from that
region. Nearby, to the southeast, sites were found with
syntopic occurrences of the two otherwise parapatric
mitochondrial subclades within clade B. This implies
that the correlation of genetic and geographic distances
for the whole data set cannot result from isolation by
distance alone, because then neither distinct clades nor
contact zones would be expected (Figs. 1 and 2). This is
also supported by the absence of evidence for isolation by
distance in the southern clade B. Therefore, we conclude
Amphib. Reptile Conserv.
Table 2. Uncorrected p distances (means, expressed as
percentages) between and within mitochondrial subclades of
Pelusios sinuatus using the cyt b gene (913 bp). Below the
diagonal are between-group values; on the diagonal, within-
group divergences are in bold.
n Al A2 A3 Bl B2
Al 2 0
A2 1 1.31 —
A3 3 Is53; 1.31 0
Bl 1B) 2.83 2.85 263 0.06
B2 21 2:15 297, 273 0.57 0.02
that the observed genetic divergence is, at least in part,
caused by vicariance and subsequent dispersal, and
that the correlation of geographic and genetic distances
results mainly from our patchy sampling. A future
challenge is to close the large sampling gaps in order to
locate additional contact zones, especially between the
northern subclades.
The north-south differentiation of P. sinuatus is similar
to that in another terrapin species. Pelusios castanoides
has a continental distribution range similar to P. sinuatus
but occurs also on Madagascar and the Seychelles
(TTWG 2017), although it is unclear whether the latter
populations are native. In P. castanoides, a sample
from the north of the distribution range (Kenya) was
distinct from samples from South Africa and southern
Mozambique (Fritz et al. 2013), suggesting a shared
biogeographic history with P. sinuatus.
To the best of our knowledge, P. sinuatus from
different parts of the distribution range have never
been compared morphologically, but northern terrapins
(clade A) seem to grow to a larger maximum size than
southern ones (clade B). According to de Witte (1952),
P. sinuatus reaches 46.5 cm in Lake Tanganyika. Branch
(2008) reports a maximum shell length of 48.5 cm for
P. sinuatus, and Spawls et al. (2002) mention up to 55
cm for upland Kenya. Serrated Hinged Terrapins of such
size are never seen in South Africa. This is confirmed
by the measurements of wild animals and collection
material reported here (Fig. 4) that show a statistically
significant difference between the mean carapace lengths
of terrapins representing clades A and B. Seven adult
museum specimens from Tanzania and Burundi (clade
A) had straight carapace lengths from 19.6 cm to 40.0 cm
(i.e., the largest specimens are still distinctly below the
published maximum size). In contrast, 14 adult museum
specimens and wild terrapins from the distribution range of
clade B (Mozambique and South Africa) ranged between
17.5 cm and 34.7 cm. Thus, it appears that northern and
southern terrapins differ morphologically, at least with
respect to their maximum size, but more measurements
are required and further studies warranted for comparing
variations in additional morphological characters. The
size variation of P. sinuatus is reminiscent of other turtles
in which size increases with latitude (Ashton and Feldman
2003), either within the same species (e.g., Chelonoidis
chilensis: Fritz et al. 2012a; Testudo graeca: Werner et al.
2016) or in distinct species of the same genus (Pelodiscus
spp.: Farkas et al. 2019). However, there are exceptions.
For instance, in Leopard Tortoises (Stigmochelys
August 2019 | Volume 13 | Number 2 | e184
Phylogeography of Pelusios sinuatus in East Africa
Table 3. Average uncorrected p distances (percentages) of 795 bp of the cyt b gene of Pe/usios species from Kindler et al. (2016).
Pelusios subniger includes a putative undescribed species from the Democratic Republic of the Congo (n = 2). It differs from other
P. subniger by an average distance of 3.13% (Petzold et al. 2014). The relationship of P. carinatus and P. rhodesianus is unclear;
some populations assigned to the latter species (P. rhodesianus A) could be conspecific with P. carinatus (Kindler et al. 2016).
Values for sympatrically occurring species pairs in boldface and red.
nig rhoA rhoB
sin
sub
upe
wil
10.91 14.01 11.82 14.99 13.56 14.56 13.54 11.80 5.43
n ada bec bro car c‘us c‘es cha cup gab mar nan
adansonii
bechuanicus 2; JLINS9
broadleyi TE e305 “1315
carinatus 15. 9:92 12.91 11.17
castaneus 19 652 13.70 7.55 11.48
castanoides 29 9.57 11.50 9.88 10.99 11.17
chapini 8 6.03 15.91 10.17 13.95 4.34 12.35
cupulatta 4 10.98 10.79 11.24 11.26 12.14 10.76 15.03
gabonensis 24 12.73 13.62 13.68 12.84 13.52 12.54 12.42 13.09
marani 5 12.80 11.21 12.68 13.01 13.57 12.50 15.35 11.82 13.75
nanus 26 11.59 14.99 15.07 15.31 15.36 12.21 12.94 14.09 12.42 15.25
niger 11.76 13.38 13.90 12.25 15.17 11.85 15.77 9.10 12.73 14.14 13.07
rhodesianus A 10.81 13.45 11.39 2.49 11.83 11.12 10.92 12.28 11.43 14.19 13.24 12.57
rhodesianusB 14 7.93 14.23 11.93 6.22 12.39 12.12 10.63 13.44 12.09 14.58 12.41 12.77 4.04
sinuatus 2 14.02 11.42 13.05 12.52 14.01 13.60 16.32 11.26 13.95 11.02 15.73 14.34 13.92 13.96
subniger 41 14.57 5.33 12.25 12.70 13.50 11.89 15.28 10.92 13.15 11.21 13.72 11.64 13.50 13.55 10.08
upembae 3 10.98 1.38 13.15 13.04 14.41 11.50 16.54
williamsi 2 915 10.91 10.87 10.23 11.03 3.89 15.00
pardalis) the northernmost and southernmost populations
comprise large-sized individuals, while tortoises from
geographically intermediate populations are medium-
sized (Fritz et al. 2010; Spitzweg et al. 2019). Another
pattern is found in continental Trachemys species once
considered conspecific, with taxa having the largest
body sizes in Central America and distinctly smaller-
sized North and South American congeners (Ernst and
Barbour 1989; Legler and Vogt 2013; Vargas-Ramirez
et al. 2017). Clearly, further research is needed for a
better understanding of the described size variation in P.
sinuatus and other turtle species, but we concur with Joos
et al. (2017) and Spitzweg et al. (2019) that many factors
beyond latitude act in concert on such variation.
An open question remains how the genetic and
morphological differentiation patterns of P. sinuatus relate
to taxonomy. The concordant variation of different genetic
and morphological characters justifies recognizing each
clade within P. sinuatus as a distinct taxon. However,
without entering the debate about species concepts and
Species conceptualization (e.g., de Queiroz 2007; Zachos
2016), we are reluctant to assign species status to either
clade. In our understanding, restricted gene flow and
largely isolated gene pools represent unambiguous
traits of distinct species. In contrast to other cases (e.g.,
Kindler et al. 2017; Spinks et al. 2014; Vamberger et al.
2015), patchy sampling prevents sound conclusions here,
particularly the lack of comprehensive sampling from the
putative contact zone of clades A and B. Yet, in times when
legislative restrictions make biodiversity research virtually
impossible for many widely distributed species (Neumann
et al. 2018; Prathapan et al. 2018), researchers are often
forced to use the evidence available as a starting point.
Amphib. Reptile Conserv.
11.01 14.11 11.33 15.73 13.69 13.97 10.77 13.31 12.28 11.31
The mitochondrial divergence of the two clades (Figs.
1 and 2), together with concordant variation in the nuclear
loci (Fig. 3), provide two important insights: (1) the two
mitochondrial clades represent distinct genealogical
lineages; and (2) mitochondrial introgression plays no
obvious role here, allowing the application of mtDNA to
infer taxonomic differentiation. Uncorrected p distances
of the mitochondrial cyt b gene have frequently been used
as a ‘taxonomic yardstick’ to decide which taxonomic
rank should be applied to turtle taxa (e.g., Iverson et al.
2013; Kindler etal. 2012, 2016; Petzold et al. 2014; Spinks
et al. 2004), analogous to the widely applied barcoding
approach (e.g., Hebert et al. 2003). However, as pointed
out by Fritz et al. (2012b) and Kindler et al. (2012), the
wide range of genetic divergences between different
turtle species (differing by one order of magnitude)
prevents the application of a rigid threshold across all
turtle groups. Instead, thresholds for different groups
need to be adjusted individually using unambiguous,
ideally sympatric, species that are closely related to the
taxa in question. Thus, previously published cyt b data
for other Pe/usios species (Kindler et al. 2016; Petzold
et al. 2014) can serve here for comparison. Also, for
these species a wide range has been reported (pairwise
average divergences between species vary from 1.38%
to 16.54%), even though the low value of 1.38% between
the allopatric P. bechuanicus and P. upembae has been
suggested to indicate their conspecificity (Kindler et al.
2016). When only divergences of sympatric species are
considered, the values range between 2.49% and 15.35%
(Table 3). Yet, the lowest value refers to P. carinatus
and populations of P. rhodesianus that could actually
be conspecific with P. carinatus (Kindler et al. 2016).
August 2019 | Volume 13 | Number 2 | e184
Vamberger et al.
If this value is disregarded, the lowest value between
unambiguous sympatric species amounts to 5.43% (P.
subniger vs. P. upembae), and this value is much higher
than the divergence between clades A and B of P. sinuatus
(2.80%) found here.
In view of this relatively low value, we suggest
subspecies status for the Serrated Hinged Terrapins
from the southernmost and more northerly parts of the
distribution range. The name Sternotherus sinuatus
Smith, 1838 is clearly referable to the southern
subspecies, while the oldest name for the northern
subspecies is Sternothaerus bottegi Boulenger, 1895 (Fig.
1). Accordingly, the smaller-sized southern populations
represent the nominotypical subspecies Pelusios
sinuatus sinuatus (Smith, 1838), and the large-sized
northern subspecies is to be named Pelusios sinuatus
bottegi (Boulenger, 1895) nov. comb. Another name,
Pelusios sinuatus zuluensis Hewitt, 1927 (type locality:
Mzinene River, KwaZulu-Natal, South Africa) clearly
is a Junior synonym of the nominotypical subspecies.
A fourth name, Pelusios sinuatus leptus Hewitt, 1933
(type locality: Isoka, Zambia) can be identified with the
northern subspecies, and is thus a junior synonym of P.
Ss. bottegi.
This assessment is in line with the recent proposal to use
the subspecies category for naming lineages that qualify
for the genetic criteria of Evolutionarily Significant Units
(ESUs; Moritz 1994). Accordingly, subspecies should
correspond to distinct mtDNA lineages (except for cases
of mitochondrial capture), and they should be diagnosable
by nuclear genomic evidence. However, in contrast to
species, subspecies are genetically less divergent and
capable of large-scale gene flow with other subspecies.
Applying subspecies names for such lineages facilitates
communication within and beyond science, particularly
in legislation and conservation (Kindler and Fritz 2018).
In this vein, the recognition of two subspecies of P.
sinuatus not only reflects their genetic divergence but also
will contribute in the medium term to their conservation.
Currently, P. sinuatus is not considered to be imperiled
(IUCN category “Least Concern,” Rhodin et al. 2018).
However, in many African countries freshwater habitats
are increasingly threatened by progressing land use and,
consequently, the numbers of Serrated Hinged Terrapins
are dwindling. Furthermore, we propose to treat the
subclades Al—A3 within P. s. bottegi and subclades B1
and B2 within P. s. sinuatus as distinct Management
Units in the sense of Moritz (1994), 1.e., as populations
with significant mitochondrial divergence.
Conclusions
Serrated Hinged Terrapins (Pelusios sinuatus) show
concordant variation in mitochondrial and nuclear
marker genes, corresponding to two distinct genealogical
lineages in the southernmost and more _ northerly
parts of the distribution range. Each lineage displays
phylogeographic structuring. Terrapins representing the
two lineages differ also in body size, with individuals
from the northern and central parts of the distribution
reaching larger sizes than terrapins from the southern
parts. Considering the degree of genetic differentiation
Amphib. Reptile Conserv.
49
compared to other Pe/usios species, we conclude that the
two lineages should be regarded as distinct subspecies.
The nominotypical subspecies Pe/usios sinuatus sinuatus
(Smith, 1838) corresponds to populations in the south
(South Africa and parts of Botswana), and the resurrected
taxon Pelusios sinuatus bottegi (Boulenger, 1895) nov.
comb. to populations from the northern and central
distribution range. A contact zone of the two subspecies is
identified in the border region of Botswana, South Africa,
and Zimbabwe. The genetically differentiated population
clusters within each subspecies should be treated as
distinct Management Units. Further research is needed
to find out whether additional diagnostic morphological
characters for the two subspecies exist. In addition, denser
sampling would allow a fine-scale phylogeography for the
Species including an assessment of gene flow between the
two subspecies and the Management Units within each
subspecies. Such research could contribute significantly
to the development of long-term management plans for
this species. However, the current legislative situation
makes progress unlikely because multiple countries are
involved and obtaining sampling permits for biodiversity
research often becomes a major, if not insurmountable,
administrative obstacle.
Acknowledgements.—We dedicate this study to the
late Bill Branch (1946-2018), who donated many of
the samples that made this investigation possible. Other
material was collected during fieldwork in South Africa.
Fieldwork and sampling in South Africa were permitted
by the Limpopo Provincial Government (permit ZA/
Lp/80202) and Ezemvelo KwaZulu-Natal Wildlife
(permits OP 5139/2012, OP 526/2014, OP 839/2014,
OP 4374/2015, OP 4092/2016, OP 139/2017, and OP
4085/2017). Terrapins sampled in the field were released at
the collection site after taking blood samples 1n accordance
with methods approved by the Ethics Committee of
the University of the Western Cape (ethical clearance
number ScRiRC2008/39) and the Animal Care, Health,
and Safety in Research Ethics Committee (AnimCare)
of the North-West University (ethical clearance number
NWU-00372-16-A5). Additional material was donated
by Werner Conradie (Port Elizabeth Museum), Peter
Praschag (Turtle Island Graz), Louis du Preez (North-
West University), Pavel Siroky (University of Veterinary
and Pharmaceutical Sciences, Brno), and Krystal Tolley
(SANBI). Angela Gaylard, Samantha Mabuza, Zelna
Silcock, and Rheinhard Scholtz (SANParks) supported
us in our South African research project applications.
We thank the Ezemvelo KwaZulu-Natal Wildlife
Permits Office and the Limpopo Provincial Government
for permits to collect biological material, and private
landowners or property managers (Annemieke and
Hermann Miller of Lapalala Wilderness Area; Kwa
Nyamazane Conservancy and Pongola River Company)
for allowing sampling on their properties. Thanks for
access to museum specimens go to Christian Klug,
Torsten Scheyer (both PIUMZ), Mark-Oliver Rodel,
Frank Tillack (both ZMB), and José Rosado (MCZ).
This paper forms part of a VLIR-UOS TEAM project
(ZEIN21013PR396), co-funded by the Water Research
Commission of South Africa (Project K5-2185, Nico J.
August 2019 | Volume 13 | Number 2 | e184
Phylogeography of Pelusios sinuatus in East Africa
Smit). Edward C. Netherlands benefitted further from
financial assistance of the National Research Foundation
(NRF), a DAAD-NRF doctoral scholarship (Grant
108803), and the VLIR-UOS university scholarship (ID
0620854/Contract 000000076310). Opinions expressed
and conclusions arrived at are those of the authors
and are not necessarily to be attributed to the funding
bodies. Genetic investigations were conducted in the
Senckenberg Dresden Molecular Laboratory (SGN-
SNSD-Mol-Lab). Thanks for laboratory work go to Anja
Rauh and Anke Miller.
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Appendix 1. Studied material of Pe/usios sinuatus and outgroups and European Nucleotide Archive (ENA) accession numbers.
Accession numbers starting with LR correspond to sequences produced for the present study.
12S cyt b ND4 Cmos R35 Rag2 Provenance Latitude Longitude As
subclade
14050 | LR594053 | LR594111 | LR594157 | LRS94218 | LR594272 | LR594325 | Botswana: Goo- -22.58402 | 27.43988 Bl
Moremi Gorge
14051 | LR594054 | LR594112 | LR594158 | LR594219 | LR594273 | LR594326 | Botswana: Goo- -22.58402 | 27.43988 Bl
Moremi Gorge
14052 | LRs94055 | LR594113 | LR594159 | LR594220 | LR594274 | LR594327 | Botswana: Goo- -22.58402 | 27.43988 Bl
Moremi Gorge
14053 | LRs94056 | LR594114 | LR594160 | LR594221 | LR594275 | LR594328 | Botswana: Goo- -22.58402 | 27.43988 Bl
Moremi Gorge
14054 | LRs94057 | LR594115 | LR594161 | LR594222 | LR594276 | LR594329 | Botswana: Goo- -22.58402 | 27.43988 Bl
Moremi Gorge
14055 | LRs94058 | LR594116 | LR594162 | LR594223 | LR594277 | LR594330 | Botswana: Goo- -22.58402 | 27.43988
Moremi Gorge
14056 | LRs94059 | LR594117 | LR594163 | LR594224 | LR594278 | LR594331 | Botswana: Goo- -22.58402 | 27.43988
Moremi Gorge
5564 | FR716875 alae FR716984 | FR717028 | FR717076 | FR717121 | Botswana: Mashatu -22.212308 | 29.136038 Pa
Game Reserve
5565 | LR594060 LR594164 | LR594225 | LR594279 | LR594332 | Botswana: Mashatu -22.212308 | 29.136038
Game Reserve
Mozambique: Cabo
7044 | LR594061 n/a LR594165 | LR594226 | LR594280 | LR594333 | Delgado: wetland at -13,089139 | 40544583 A2
southern end of Pemba
drainage (Pemba)
Mozambique: Cabo
7045 | LRS94062 n/a LR594166 | LR594227 n/a Delgado: wetland at -13.089139 | 40.544583
southern end of Pemba
drainage (Pemba)
Mozambique: Cabo
7046 | LR594063 n/a LR594167 | LR594228 LR594334 | Delgado: wetland at -13.089139 | 40.544583
southern end of Pemba
drainage (Pemba)
Mozambique: Cabo
7047. | LRS94064 n/a LR594168 | LR594229 Delgado: wetland at -13.089139 | 40.544583
southern end of Pemba
drainage (Pemba)
Mozambique: Cabo
7049 | LRS94066 n/a LR594170 | LR594230 LR594335 | Delgado: wetland at -13,089139 | 40.544583
southern end of Pemba
drainage (Pemba)
17104 | LR594067 | LR594118 | LR594171 | LR594231 | LR594281 | LR594336 | Mozambique: Cabo -11.884827 } 40.460208
Delgado: Rio Diquide
LRS94282 Mozambique: Sofala
9891 LR594068 n/a LR594172 | LR594232 LR594337 | province, along road -20.923567 34.6662
LR594283 OR
August 2019 | Volume 13 | Number 2 | e184
Bales
Mozambique: Cabo
7048 | LRS594065 n/a LR594169 n/a n/a Delgado: wetland at -13.089139 | 40.544583 A2
southern end of Pemba
drainage (Pemba)
Amphib. Reptile Conserv. 52
Vamberger et al.
Appendix 1 (continued). Studied material of Pe/usios sinuatus and outgroups and European Nucleotide Archive (ENA) accession
numbers. Accession numbers starting with LR correspond to sequences produced for the present study.
12S cyt b ND4 Cmos R35 Rag2 Provenance Latitude Longitude a
subclade
Mozambique: Sofala
11100 LR594069 n/a LR594173 | LR594233 | LR594284 | LR594338 | province, along road -21.007317 | 34.539433 Al
428
LRS94285 Mozambique: Sofala:
6956 LR594070 | LR594119 | LR594174 | LR594234 LR594286 LR594339 | NE of Rio Save Game -20.933333 | 34.316667 Al
Reserve
a
Mozambique: Sofala:
6959 | LR594071 | LR594120 | LR594175 | LR594235 | LR594287 | LR594340 | NE of Rio Save Game -20.7425 34.586567 Al
Reserve
5215 | LRS594072 n/ LR594176 | LR594236 | LRS594288 | LR594341 Mozambique: -17.059513 | 38.699233 A2
Zambesia: Moebase
South A frica:
17003 | LR594073 | LR594121 | LR594177 | LR594237 | LR594289 | LR594342 | KwaZulu-Natal: -28.05752 | 32.29332 B2
Bonamanzi Game
Reserve
South A frica:
17004 | LR594074 | LR594122 | LR594178 | LR594238 | LR594290 | LR594343 | KwaZulu-Natal: -28.05752 | 32.29332 B2
Bonamanzi Game
Reserve
South A frica:
17005 | LR594075 | LR594123 | LR594179 | LR594239 | LR594201 | LR59434q | KwaZulu-Natal: -28.05752 | 32.29332 B2
Bonamanzi Game
Reserve
South A frica:
17006 | LR594076 } LR594124 | LR594180 | LR594240 | LR594292 | LRso434s | KwaZulu-Natal: -28.05752 | 32.29332 B2
Bonamanzi Game
Reserve
South Africa:
17010 | LR594077 | LR594125 | LR594181 n/a n/a nae) _ | eee al -28.145899 | 31.591881 B2
Bonamanzi Game
Reserve
South A frica:
9143. | LR594078 | LR594126 | LR594182 | LR594241 | LR594293 | LRs9o4346 | KwaZulu-Natal: -28.05809 | 32.29412 B2
Bonamanzi Game
Reserve, Waterlily Dam
South A frica:
14040 | LR594079 | LR594127 | LR594183 | LR594242 | LR594204 | LR594347 | KwaZulu-Natal: Jozini, | 57 591656 | 3.139094 B2
Kwa Nyamazane
Conservancy
South Africa:
KwaZulu-Natal:
16199 LR594080 | LR594128 | LR594184 | LR594243 | LR594295 LR594348 | Manyiseni region in -26.876389 | 32.011389 B2
Lebombo Mountains,
near Mabona
South Africa:
KwaZulu-Natal:
16200 LR594081 | LR594129 | LR594185 | LR594244 | LR594296 | LR594349 | Manyiseni region in -26.876389 | 32.011389 B2
Lebombo Mountains,
near Mabona
South Africa:
KwaZulu-Natal:
16202 LR594082 | LR594130 | LR594186 | LR594245 | LR594297 | LR594350 | Manyiseni region in -26.876389 | 32.011389 B2
Lebombo Mountains,
near Mabona
South A frica:
KwaZulu-Natal:
16203 LR594083 | LR594131 | LR594187 | LR594246 | LR594298 | LR594351 | Manyiseni region in -26.876389 | 32.011389 B2
Lebombo Mountains,
near Mabona
South Africa:
10614 LR594084 n/a LR594188 | LR594247 | LR594299 | LR594352 | KwaZulu-Natal: -26.885692 | 32.223672 B2
Ndumo Game Reserve
South Africa:
10615 LR594085 | LR594132 | LR594189 | LR594248 | LR594300 | LR594353 | KwaZulu-Natal: -26.874944 | 32.231997 B2
Ndumo Game Reserve
South Africa:
14041 LR594086 | LR594133 | LR594190 | LR594249 | LR594301 LR594354 | KwaZulu-Natal: -26.891275 32.299 B2
Ndumo Game Reserve
Amphib. Reptile Conserv. 53 August 2019 | Volume 13 | Number 2 | e184
Phylogeography of Pelusios sinuatus in East Africa
Appenidx 1 (continued). Studied material of Pe/usios sinuatus and outgroups and European Nucleotide Archive (ENA) accession
numbers. Accession numbers starting with LR correspond to sequences produced for the present study.
12S cyt b ND4 Cmos R35 Rag2 Provenance Latitude Longitude ae
subclade
South Africa:
13590 LR594087 | LR594134 | LR594191 | LR594250 | LR594302 | LR594355 KwaZulu-Natal: ; -26.865118 | 32.240964
Ndumo Game Reserve:
Mabayani
South Africa:
FR716876 FR716937 | FR716985 | FR717029 FR717077 FR717122 | KwaZulu-Natal: Phinda | -27.843744
Game Reserve
South Africa:
FR716877 | FR716938 | FR716986 | FR717030 | FR717078 FR717123 | KwaZulu-Natal: Phinda | -27.843744
Game Reserve
South Africa:
LR594088 | LR594135 | LR594192 | LR594251 | LR594303 | LR594356 | KwaZulu-Natal: St. -28.357158
Lucia: Crocodile Centre
South Africa:
LR594089 | LR594136 | LR594193 | LR594252 | LR594304 | LR594357 | KwaZulu-Natal: St. -28.357158
Lucia: Crocodile Centre
South Africa:
LR594090 | LR594137 | LR594194 | LR594253 | LR594305 LR594358 | KwaZulu-Natal: St. -28.357158
Lucia: Crocodile Centre
South Africa: Limpopo:
LR594091 | LR594138 | LR594195 | LR594254 | LR594306 | LR594359 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594092 | LR594139 | LR594196 | LR594255 | LR594307 | LR594360 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594093 | LR594140 | LR594197 | LR594256 | LR594308 | LR594361 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594094 | LR594141 | LR594198 | LR594257 | LR594309 | LR594362 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594095 | LR594142 | LR594199 | LR594258 | LR594310 | LR594363 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594096 | LR594143 | LR594200 | LR594259 | LR594311 LR594364 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594097_ | LR594144 | LR594201 | LR594260 | LR594312 | LR594365 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594098 | LR594145 | LR594202 | LR594261 | LR594313 LR594366 | Hoedspruit: Bush -24.35039
Pub Inn
South Africa: Limpopo:
LR594099 | LR594146 | LRS594203 | LR594262 | LRS594314 | LR594367 | Hoedspruit: Bush -24 35039
Pub Inn
LR594100 | LR594147 | LR594204 | LR594263 | LR594315 | LR594368 ea oe Limpopo: | _53 9392
LR594101 | LR594148 | LR594205 | LR594264 | LR594316 | LR594369 eae Limpopo: | _53 39392
South Africa: Limpopo:
LR594102 | LR594149 | LR594206 | LR594265 | LR594317 | LR594370 | Palabora Mining -24.018889
Company, near Loolo
Dam, S of Phalaborwa
South Africa: Limpopo:
LR594103 | LR594150 | LR594207 | LR594266 | LR594318 | LR594371 | Palabora Mining
Company, SE of
Phalaborwa
South Africa: Limpopo:
LR594104 | LR594151 | LR594208 n/a LR594319 | LR594372
Palabora Mining
LR594105 | LR594152 | LR594209
5216 32.335521
32.335521
17014 32.419512
17015 32.419512
17016 32.419512
17028 31.152019
17029 31.152019
17030 31.152019
17031 31.152019
17038
17039 31.152019
17040 31.152019
17041 31.152019
17042 31.152019
17061 28.29516
17068 28.29516
31.140833
Ne)
aS
31.210556
Company: Cleveland
Nature Reserve, in
Olifants River near
picnic site
LR594267 | LR594320 | LR594373 | South Africa: Limpopo: | _53 98716
Vaalwater
-24.03056 31.19306
B2
B2
B2
B2
B2
B2
B2
B2
B2
B2
Bl
B2
B2
B2
Bl
Bl
Bl
Bl
Bl
B2
1
17073
Amphib. Reptile Conserv. 54 August 2019 | Volume 13 | Number 2 | e184
Vamberger et al.
Appenidx 1 (continued). Studied material of Pelusios sinuatus and outgroups and European Nucleotide Archive (ENA) accession
numbers. Accession numbers starting with LR feel to sequences produced for the present study.
s , mtDNA
LR594210
South Africa:
Mpumalanga: Kruger
13585 LR594106 | LR594153 LR594268 | LR594321 | LR594374 | National Park: -23.107365 | 31.439066 Bl
Shingwedzi River near
Shingwedzi Camp
South Africa:
Mpumalanga: Kruger
13586 LR594107 n/a LR594211 National Park: -23.107365 | 31.439066 Bl
Shingwedzi River near
Shingwedzi Camp
16214 | LR594108 | LR594154 | LR594212 | LR594269 | LR594322 | LR594375 Bae -3.34261 | 37319831
Tanzania: Manyara
16269 LR594109 | LR594155 | LR594213 | LR594270 | LR594323 | LR594376 | Region: Kikuletwa -3.443532 37.193393 A3
Hotsprings
Tanzania: Manyara
16270 LR594110 | LR594156 | LR594214 | LR594271 | LR594324 | LR594377 | Region: Kikuletwa -3.443532 37.193393 A3
Hotsprings
|_| Outgroups
Pelusios marani
Pelomedusa variabilis
Amphib. Reptile Conserv. 55 August 2019 | Volume 13 | Number 2 | e184
Amphib. Reptile Conserv.
Phylogeography of Pelusios sinuatus in East Africa
Melita Vamberger is a Slovenian herpetologist and evolutionary biologist working at the Senckenberg
Natural History Collections, Dresden, Germany. Melita studied Biology at the University of Ljubljana,
Slovenia, focusing on the natural history of the European Pond Turtle (Emys orbicularis). After
her diploma, Melita moved to Germany for her Ph.D. at the University of Leipzig, studying the
phylogeography and hybridization of two closely related freshwater turtle species (Mauremys caspica
and M. rivulata). Melita’s main interests are speciation, gene flow, adaptation, and evolution of different
turtle taxa using an integrative approach that combines genetic and ecological methods, especially in
the Western Palearctic and sub-Saharan Africa.
Margaretha D. Hofmeyr is Professor Emeritus at the Biodiversity and Conservation Biology
Department, University of the Western Cape, South Africa. Margaretha is an ecophysiologist by
training, and first studied large ungulates before switching to chelonians. Her ecophysiological
studies revealed that South African tortoises have many unique characteristics, which stimulated
further interest in their genetic diversity and systematics. Margaretha has published extensively on
the ecology and phylogeography of sub-Saharan tortoises and turtles, and she is closely involved in
conservation projects for threatened tortoises. This work resulted in her being awarded the 2015 Sabin
Turtle Conservation Prize. Margaretha is a member and Regional Vice-Chair for Africa of the IUCN/
SSC TFTSG and coordinated the 2014 and 2018 Red List Assessments for South African tortoises and
freshwater turtles.
Courtney A. Cook is a Senior Lecturer in the Water Research Group, Unit for Environmental Sciences
and Management, North-West University, South Africa. Courtney is a parasitologist focusing on
the biodiversity, taxonomy, and phylogeny of protozoan blood parasites of ectothermic vertebrates
(amphibians, reptiles, and fish), with several authored and co-authored scientific articles in this area. Her
M.Sc. and Ph.D. both focused exclusively on these parasites infecting tortoises of South Africa, which
inspired a keen interest in these animals, particularly with respect to their taxonomy and phylogeny,
both important aspects in understanding the associated host-parasite relationships. Courtney was
recently awarded a Y-rating by the South African National Research Foundation, identifying her as a
promising young researcher in her field from a global perspective.
Edward C. Netherlands is a dual Ph.D. candidate between the North-West University, South Africa,
and Katholieke Universiteit Leuven, Belgium. His Ph.D. forms part of the VLIR-UOS program for
the development of tools for the sustainable utilization and management of aquatic resources in
South Africa. Edward’s research interests focus on the molecular biology, ecology, and taxonomy
of herpetofauna and their associated parasites. He is also passionate about teaching the importance
of conservation to young minds and non-scientists. Ed has authored or co-authored several scientific
articles and a bilingual frog field guide (in English and Zulu). Edward also received the Research
Excellence for Next Generation Researchers Award as a final year Ph.D. Candidate from the National
Research Foundation in South Africa.
Uwe Fritz is the head of the Museum of Zoology, Senckenberg Natural History Collections in Dresden,
Germany, and Extraordinary Professor for zoology at the University of Leipzig, Germany. Uwe has
worked for many years on the taxonomy, systematics, and phylogeography of turtles and tortoises,
and has also studied snakes and lizards to a lesser extent. He is particularly interested in hybridization
patterns and gene flow in the contact zones of distinct taxa. Uwe has authored or co-authored numerous
scientific articles, mainly in herpetology, and has edited proceedings and books, among them the two
turtle volumes of the Handbook of Amphibians and Reptiles of Europe.
56 August 2019 | Volume 13 | Number 2 | e184
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 57-60 (e185).
Mind the gap—ls the distribution range of Pelomedusa
galeata really disjunct in western South Africa?
‘Melita Vamberger, ‘Paula Ribeiro Anunciagao, *Margaretha D. Hofmeyr, and ‘Uwe Fritz
'Museum of Zoology, Senckenberg Natural History Collections Dresden, A.B. Meyer Building, 01109 Dresden, GERMANY ?Chelonian Biodiversity
and Conservation, Department of Biodiversity and Conservation Biology, University of the Western Cape, Bellville 7535, SOUTH AFRICA
Abstract.—Records from the putative gap in the distribution range of Pelomedusa galeata in western South
Africa provide evidence for the occurrence of helmeted terrapins in those areas. Further research is needed to
reveal the genetic and taxonomic identity of these populations.
Keywords. helmeted terrapin, Northern Cape Province, Pelomedusidae, Testudines, turtle
Citation: Vamberger M, Anunciagao PR, Hofmeyr MD, Fritz U. 2019. Mind the gap—ts the distribution range of Pelomedusa galeata really disjunct in
western South Africa? Amphibian & Reptile Conservation 13(2) [Special Section]: 57-60 (e185).
Copyright: © 2019 Vamberger et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 28 February 2019; Accepted: 22 March 2019; Published: 20 August 2019
Helmeted terrapins have a wide distribution across sub-
Saharan Africa and the southwestern Arabian Peninsula.
Together with their sister taxon, the African hinged
terrapins (Pelusios), helmeted terrapins constitute the
side-necked turtle family Pelomedusidae (TTWG 2017).
While it was assumed for decades that all helmeted
terrapins are conspecific (Boycott and Bourquin 2008;
Branch 2008; Ernst and Barbour 1989; Wermuth and
Mertens 1961, 1977), several investigations revealed
deep genetic divergences between geographically
coherent populations, which resemble or exceed the
divergences of distinct Pe/usios species (Fritz et al. 2011,
2014; Petzold et al. 2014; Vamberger et al. 2018; Vargas-
Ramirez et al. 2010; Wong et al. 2010). This resulted in
the formal recognition of no less than 10 distinct species
(Petzold et al. 2014; TTWG 2017; Vamberger et al. 2018).
In addition to these, a minimum of five unnamed species
are thought to exist, which are characterized by similar
genetic divergences but otherwise only insufficiently
known (Fritz et al. 2015; Nagy et al. 2015; Petzold et
al. 2014; Vamberger et al. 2018; Vargas-Ramirez et al.
2016).
In the Southern African region south of the Cunene
and Zambezi Rivers, two species are known to occur,
the South African Helmeted Terrapin Pelomedusa
galeata (Schoepff, 1792) and the Common Helmeted
Terrapin Pelomedusa subrufa (Bonnaterre, 1789) (Fritz
et al. 2015; Petzold et al. 2014; Vamberger et al. 2018).
Pelomedusa galeata is distributed in most of South Africa
and replaced in the countries north of South Africa by
P. subrufa, which enters also northeastern South Africa
(provinces of Limpopo and Mpumalanga). In these
Correspondence. * wve.fritz@senckenberg.de
Amphib. Reptile Conserv.
57
provinces, the distribution ranges of the two species
abut and the closest records of P. galeata and P. subrufa
are separated only by 80 km, so that overlapping ranges
seem possible (Vamberger et al. 2018). Pelomedusa
galeata shows pronounced phylogeographic structuring,
with two genetically deeply divergent groups in the east
and west of South Africa that most likely represent two
distinct species. The eastern group is phylogeographically
structured, with three parapatric subgroups (Fritz et al.
2015; Petzold et al. 2014; Vamberger et al. 2018).
Detailed distribution maps for helmeted terrapins show
a patchy range for Southern Africa, with large putative
gaps in western South Africa, southern Mozambique,
southern Namibia, and most of Botswana (Boycott 2014;
Boycott and Bourquin 2008; TTWG 2017). Except
for southern Mozambique, these regions are very arid,
suggestive of pessimal conditions for a freshwater turtle
like the helmeted terrapin. However, P. subrufa is known
to cope with year-long drought. In Namibia (Omaheke),
terrapins of this species may evidently survive up to six
years burrowed in the soil (Petzold et al. 2014) and surface
only after the rare rainfalls. Boycott and Bourquin (2008)
suggested that helmeted terrapins take advantage of man-
made farm dams and expanded their range into otherwise
unsuitable regions, including semi-desert. However,
records for P subrufa from the mouths of temporary
streams in the Namib Desert may well represent natural
occurrences of terrapins washed downstream during the
rare floods there (A. Schleicher, pers. comm. ).
One large distribution gap is located in western
South Africa and concerns P. galeata. It more or less
separates the two genetically deeply divergent groups of
this species (Vamberger et al. 2018). During fieldwork
in October and November 2018, the first two authors
August 2019 | Volume 13 | Number 2 | e185
Distribution of Pelomedusa galeata in South Africa
pS
ere Se A . ae
Fig. 1. Pelomedusa galeata Rott if Ratelfontein farm near Calvinia observed directly after eal 16 February 2019. For the
location of the farm, see Fig. 2 (locality 1). Photos: C.A. van Niekerk.
Northern Cape
Western Cape
O
North West
Free State
Fig. 2. Distribution range of Helmeted Terrapins (shaded in grey), with our records of Pelomedusa galeata in South Africa (white
circles). New records of P. galeata in or close to the putative distribution gap: 1 — Nineteen turtles at Ratelfontein farm, near
Calvinia (16 February 2019), 2 — Observations of locals at Williston, 3 — Near Carnarvon (shell, collected 25 October 2018), 4— One
terrapin near Beaufort West (4 March 2017), 5 — Two terrapins near Griekwastad (28 October 2018). Inset: Pelomedusa galeata
from the Ratelfontein farm. Photo: C.A. van Niekerk.
had the opportunity to examine parts of this putative
distribution gap for the presence of helmeted terrapins. In
addition to direct observations, interviews with farmers
and locals contributed further information. It is common
knowledge there that helmeted terrapins are present but
very scarce. They are seen only after the rare rainfall
events, when the terrapins are walking to waterholes (Fig.
1). Together with our records substantiated by specimens,
Amphib. Reptile Conserv.
this provides the first evidence for the occurrence of P.
galeata in the central part of the Northern Cape Province
of South Africa (Fig. 2). We assume that the helmeted
terrapin has an even wider distribution and also occurs
northwards to Namibia, and that a distribution gap does
not exist at all. Pelomedusa are very elusive animals
in arid regions, and we presume that the putative gap
reflects not a real absence of helmeted terrapins but
August 2019 | Volume 13 | Number 2 | e185
Vamberger et al.
a lack of records. Further research is needed to reveal
which genetic lineage of P galeata occurs in this area
and whether there is a contact zone of the two lineages
currently identified with P. galeata.
Acknowledgements.-We would like to thank C.A. and
Berno van Niekerk from Ratelfontein farm, Adam van
Greunen, Isak Dreyer, Pieter and Elmarie Naude from
Die Ark, Rodney Bartholomew, Haas van Niekerk,
Bertus and Roux Steenkamp, Nadia and Abri van Zyl,
Adriaan Jordaan, Nick Telford, and Krystal Tolley for
all the valuable information, pictures, and help during
fieldwork. Fieldwork of M.V. and P.R.A. was supported
by the DGHT (Deutsche Gesellschaft fir Herpetologie
und Terrarienkunde) and the BCG (British Chelonian
Group). M.D.H. was supported by the Mapula Trust.
Fieldwork was permitted by the North West Province
(NW 6124/10/2018) and Northern Cape Province
(0729/2018 and 0730/2018).
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Boycott RC, Bourquin O. 2008. Pelomedusa subrufa
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M, Vences M, et al. 2011. Molecular phylogeny of
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Fritz U, Kehlmaier C, Mazuch T, Hofmeyr MD, du
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M, Branch WR, du Preez L, Hofmeyr MD, Meyer L,
Schleicher A, Siroky P, etal. 2014. Arevision of African
helmeted terrapins (Testudines: Pelomedusidae:
Pelomedusa), with descriptions of six new species.
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TTWG (Turtle Taxonomy Working Group), Rhodin AGJ,
Iverson JB, Bour R, Fritz U, Georges A, Shaffer HB,
van Dik PP. 2017. Turtles of the World. Annotated
Checklist and Atlas of Taxonomy, Synonymy,
Distribution, and Conservation Status. 8th edition.
Chelonian Research Monographs 7. Chelonian
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USA. 292 p.
Vamberger M, Hofmeyr MD, Ihlow F, Fritz U. 2018.
In quest of contact: phylogeography of helmeted
terrapins (Pelomedusa galeata, P. subrufa sensu
stricto). PeerJ 6: e4901.
Vargas-Ramirez M, Petzold A, Fritz U. 2016. Distribution
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316.
Vargas-Ramirez M, Vences M, Branch WR, Daniels
SR, Glaw F, Hofmeyr MD, Kuchling G, Maran J,
Papenfuss T, Siroky P, et al. 2010. Deep genealogical
lineages in the widely distributed African Helmeted
Terrapin: evidence from mitochondrial and nuclear
DNA _ (Testudines: Pelomedusidae: Pelomedusa
subrufa). Molecular Phylogenetics and Evolution 56:
428-440.
Wermuth H, Mertens R. 1961. Schildkréten, Krokodile,
Briickenechsen. VEB Gustav Fischer Verlag, Jena,
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Rhynchocephalia. Das Tierreich 100: 1-174.
Wong RA, Fong JJ, Papenfuss TJ. 2010. Phylogeography
of the African Helmeted Terrapin, Pelomedusa
subrufa. genetic structure, dispersal, and human
introduction. Proceedings of the California Academy
of Sciences 61: 575-585.
August 2019 | Volume 13 | Number 2 | e185
Amphib. Reptile Conserv.
Distribution of Pelomedusa galeata in South Africa
Melita Vamberger is a Slovenian herpetologist and evolutionary biologist working at the Senckenberg
Natural History Collections, Dresden, Germany. Melita studied Biology at the University of Ljubljana,
Slovenia, focusing on the natural history of the European Pond Turtle (Emys orbicularis). After her
diploma, she moved to Germany for her Ph.D. at the University of Leipzig on the phylogeography
and hybridization of two closely related freshwater turtle species (VMauremys caspica and M. rivulata).
Melita’s main interests are speciation, gene flow, adaptation, and evolution of different turtle taxa using an
integrative approach that combines genetic and ecological methods, especially in the Western Palearctic
and sub-Saharan Africa.
Paula Ribeiro Anunciac4o is a Brazilian ecologist and herpetologist. She is mainly interested in the
consequences of human disturbance for tropical amphibian communities. Paula studied biology at the
Federal University of Alfenas, Minas Gerais, Brazil. There, she also earned her master’s degree in
Ecology and examined the influence of matrix types and habitat fragmentation on the amphibian diversity
of the Atlantic rainforest. Paula earned her Ph.D. in Applied Ecology at the Federal University of Lavras,
Minas Gerais, Brazil, in 2018. For her Ph.D., she studied the relationships of land use change, climate
change, and taxonomic and functional richness of amphibians, which included some months of work at
the Senckenberg Natural History Collections, Dresden, Germany.
Margaretha D. Hofmeyr is Professor Emeritus at the Biodiversity and Conservation Biology
Department, University of the Western Cape, South Africa. She is an ecophysiologist by training and first
studied large ungulates before switching to chelonians. Her ecophysiological studies revealed that South
, African tortoises have many unique characteristics, which stimulated her interest in their genetic diversity
and systematics. Margaretha has published extensively on the ecology and phylogeography of sub-
Saharan tortoises and turtles, and she is closely involved in conservation projects that focus on threatened
tortoises. This work resulted in her being awarded the 2015 Sabin Turtle Conservation Prize. Margaretha
is amember, and Regional Vice-Chair for Africa, of the IUCN/SSC TFTSG and she coordinated the 2014
and 2018 Red List Assessments for South African tortoises and freshwater turtles.
Uwe Fritz is the head of the Museum of Zoology, Senckenberg Natural History Collections at Dresden,
Germany, and Extraordinary Professor for Zoology at the University of Leipzig, Germany. He has worked
for many years on the taxonomy, systematics, and phylogeography of turtles and tortoises, and also
studied to a lesser extent snakes and lizards. Uwe is particularly interested in hybridization patterns and
gene flow in contact zones of distinct taxa. He has authored or co-authored numerous scientific articles,
mainly in herpetology, and has also edited proceedings and books, among them the two turtle volumes of
the Handbook of Amphibians and Reptiles of Europe.
60 August 2019 | Volume 13 | Number 2 | e185
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 61-67 (e195).
Geographic range extension of Speke’s
Hinge-back Tortoise Kinixys spekii Gray, 1863
1*Flora lhlow, 2**°Harith M. Farooq, °Vaclav Gvozdik, ‘Margaretha D. Hofmeyr, ®°Werner Conradie,
‘Patrick D. Campbell, “James Harvey, ‘*Luke Verburgt, and ‘Uwe Fritz
'Museum of Zoology, Senckenberg Dresden, A. B. Meyer Building, 01109 Dresden, GERMANY *Faculty of Natural Sciences, Lurio University, Pemba
958, MOZAMBIQUE Gothenburg Global Biodiversity Centre, 40530 Gothenburg, SWEDEN *Department of Biology and CESAM, University of
Aveiro, 3810-193 Aveiro, PORTUGAL *Department of Biological and Environmental Sciences, University of Gothenburg, 40530 Gothenburg, SWEDEN
°Institute of Vertebrate Biology of the Czech Academy of Sciences, 60365 Brno, CZECH REPUBLIC ‘Chelonian Biodiversity and Conservation,
Department of Biodiversity and Conservation Biology, University of the Western Cape, Bellville 7535, SOUTH AFRICA *Port Elizabeth Museum
(Bayworld), P.O. Box 13147, Humewood 6013, SOUTH AFRICA °School of Natural Resource Management, George Campus, Nelson Mandela
University, George 6530, SOUTH AFRICA '°Department of Life Sciences, Natural History Museum, London, UNITED KINGDOM ''41 Devonshire
Avenue, Howick, 3290, SOUTH AFRICA '*Department of Zoology and Entomology, University of Pretoria, Pretoria, 0001, SOUTH AFRICA
Abstract.—Kinixys spekii has a wide distribution range across sub-Saharan Africa, having been reported from
Angola, Botswana, Burundi, the Democratic Republic of the Congo, eSwatini, Kenya, Malawi, Mozambique,
Namibia, South Africa, Tanzania, Zambia, and Zimbabwe. Kinixys spekii inhabits savannah and dry bushveld
habitats and was previously considered an inland species. However, recent records suggest a more extensive
geographical distribution. Here, we provide genetically verified records for Angola, South Africa, and
Mozambique, and discuss reliable sightings for Rwanda. These new records extend the range significantly to
the east and west, and provide evidence for the occurrence of this species along the coast of the Indian Ocean
in South Africa and Mozambique.
Keywords. Africa, Angola, chelonians, distribution, Mozambique, Reptilia, Rwanda, Testudinidae
Citation: lhlow F, Farooq HM, Gvozdik V, Hofmeyr MD, Conradie W, Campbell PD, Harvey J, Verburgt L, Fritz U. 2019. Geographic range extension
of Speke’s Hinge-back Tortoise Kinixys spekii Gray, 1863. Amphibian & Reptile Conservation 13(2) [Special Section]: 61-67 (e195).
Copyright: © 2019 lhlow et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 17 July 2019; Accepted: 28 September 2019; Published: 6 November 2019
The genus Kinixys currently comprises eight species
(Kindler et al. 2012; TTWG 2017): K. belliana Gray,
1830; K. erosa (Schweigger, 1812); K. homeana
Bell, 1827; K. lobatsiana Power, 1927; K. natalensis
Hewitt, 1935; K. nogueyi (Lataste, 1886); K. spekii
Gray, 1863; and K. zombensis Hewitt, 1931. Two of
these species are confined to rainforest habitats (K.
erosa, K. homeana), while one is restricted to north-
western Africa (K. nogueyi), and the remaining five
occupy savannah and forest habitats in eastern and
south-eastern Africa.
Speke's Hinge-back Tortoise, Kinixys spekii, has an
extensive geographical distribution range, spanning
twelve countries, from southern Kenya southward to
eSwatini (formerly Swaziland), southern Mozambique,
and north-eastern South Africa, where it reaches its
southernmost limit (Boycott and Bourquin 2000; Branch
et al. 1995; Broadley 1989a; Spawls et al. 2004, 2018;
TTWG 2017). The species’ westward range extends
across Zimbabwe, Zambia, and northern Botswana
into the Zambezi (formerly Caprivi) region of Namibia
(Broadley 1989a, 1993; Jacobsen et al. 1986; Pienaar
et al. 1983; TTWG 2017). According to Broadley
(1989a,b, 1993), K. spekii is confined to the inland parts
of southern and central Africa, inhabiting the eastern
plateau slopes, while the range of K. zombensis extends
along the East African coastal plain from Kenya to the
KwaZulu-Natal Province of South Africa. However,
a few records from Kenya (Watamu, 3.34250°S,
40.02740°E; in the vicinity of Kilifi, voucher specimen
in the collection of the Yale Peabody Museum of
Natural History YPM HERR 014516) suggest that the
range of K. spekii reaches the northern coastal areas as
well. Since some photographs of tortoises from Watamu
shown in Spawls et al. (2004, 2018) morphologically
resemble K. zombensis rather than K. spekii, this record
requires verification.
In terms of habitat, K. spekii has been recorded from
savannah, tropical bushveld, tropical savannah, sour
bushveld, and the thornveld of the Lebombo Plateau
Correspondence. flora.ihlow@senckenberg.de (*F1), harithmorgadinho@gmail.com (HMB), vaclav.gvozdik@ivb.cz (VG),
mdhofmeyr@gmail.com (MDH), werner@bayworld.co.za (WC), p.campbell@nhm.ac.uk (PDC), info@harveyecological.co.za (JH),
luke@enviro-insight.co.za (LV), uwe.fritz@senckenberg.de (UF)
Amphib. Reptile Conserv.
November 2019 | Volume 13 | Number 2 | e195
Distribution of Kinixys spekii in Africa
(Boycott 2001; Boycott and Bourquin 2000; Branch
2008). According to Broadley (1989a), this species
prefers moist savannah woodlands, such as Miombo and
Mopane (woodlands dominated by Brachystegia and
Colophospermum species, respectively), but also occurs
in drier deciduous woodlands and thickets dominated
by Vachellia (until recently Acacia; Kyalangalilwa et al.
2013) and Commiphora in the north-eastern part of its
range (Broadley 1989a).
For the present contribution, records for K. spekii
were compiled from the scientific literature and
museum collections, and supplemented with a few
selected sightings from the online Virtual Museum
Database Naturalist (https://www.inaturalist.org) to
discuss the distribution range of K. spekii. Several new
and genetically verified records from Angola, South
Africa, and coastal Mozambique are also presented,
which extend the species’ known distribution range
considerably. Genetic verification relied on an mtDNA
sequence coding for the partial NADH dehydrogenase
subunit 4 (ND4) and adjacent tRNAs.
Unfortunately, online databases and data aggregators
are often compromised by incorrect identifications and
outdated taxonomy, and either provide no photographic
vouchers or ones that are unsuitable for facilitating
verification before using the data. Nevertheless, two
photographic vouchers deposited with Naturalist
(https://www. inaturalist.org/observations/18255494,
https://www. inaturalist.org/observations/1047117) could
clearly be assigned to K. spekii, based on characteristic
coloration patterns and shell shape. These records
provide evidence that the species occurs as far north-
west as Nyagatare (1.42321°S, 30.63027°E) and
Akagera (1.55162°S, 30.60760°E) in Rwanda, which
is in accordance with Spawls et al. (2004, 2018), who
reported isolated records for K. spekii from Akagera, the
Ruzizi Plain, and the southern Kerio Valley in eastern
Rwanda. To the east, two genetically verified K. spekii
(Museum of Zoology, Senckenberg Dresden, Tissue
Collection: MTD 17106, 17107; European Nucleotide
Archive accession numbers: LR723010, LR723011)
were sampled and released by Luke Verburgt in February
2014 on the Afungi Peninsula, Cabo Delgado Province,
coastal Mozambique (10.81939°S, 40.54842°E; but see
below). In addition, four genetically verified adult K.
spekii (MTD 20463, 20464; LR723016, LR723017) were
sampled and released by Harith M. Faroog within a 10 km
radius of the Lurio University in Pemba, Cabo Delgado
Province, Mozambique (12.97540°S, 40.57083°E) in
2014. An adult female (12.97615°S, 40.10205°E) and
an adult male tortoise (12.99333°S, 39.94861°E) were
sampled and released by William R. Branch in March
2017 in Ancuabe, Cabo Delgado Province, Mozambique,
and both were genetically verified to represent K. spekii
(MTD 20463-20464; LR723016-7). In the west, a genetic
sample (SANBI 2126; LR723018) collected by Thomas
Branch in October 2008 shows that K. spekii also occurs
Amphib. Reptile Conserv.
near Saurimo, Lunda Sul Province, Angola (9.39694°S,
20.43194°E).
With the exception of the tortoises from the Afungi
Peninsula, all specimens could unambiguously be
identified morphologically as K. spekii based on the
following characteristics: beak unicuspid, carapace with
well-developed hinge, carapace distinctly depressed,
and posterior marginal scutes not recurved or serrated.
Previous records for Mozambique were limited to the
southwest (Boycott and Bourquin 2000), the vicinity
of Ressano Garcia, southern Mozambique (Broadley
1989b), and the Maputo Elephant Reserve situated along
the coast of southern Mozambique (voucher specimen in
the collection of the Ditsong National Museum of Natural
History TM 41761; Broadley 1993; Fig. 1). To the south,
samples collected in the KwaZulu-Natal Province, South
Africa, were genetically verified as K. spekii (MTD
13594 from Mkhuze Game Reserve; LR723019; MTD
7457 from the vicinity of Mtubatuba; HE662316).
Previously, K. spekii was only known from the extreme
northern border of the province, adjacent to eSwatini and
Mozambique (Bourquin 2004; Boycott 2014).
The abovementioned records enlarge the known
geographical distribution range of K. spekii, but also
demonstrate that the species’ distribution range is still
incompletely known. Unfortunately, morphological
traits overlap between Kinixys species, making
species identification in potential zones of sympatry
extremely difficult. For instance, K. spekii co-occurs
with K. zombensis in the Maputo Elephant Reserve in
Mozambique, and the Ndumo Game Reserve in South
Africa. In the Waterberg area of South Africa K. spekii
is found close to K. lobatsiana populations, and it was
recorded together with K. natalensis in the vicinity of
Jameson’s Drift, in the Lebombo Mountains in KwaZulu-
Natal as well as in the area of Hoedspruit. In these areas,
hybridization is possible, which further complicates
identification. For example, the two tortoises collected
from the Afungi Peninsula in northern Mozambique
morphologically resemble K. zombensis (Fig 3;
domed carapace, radial coloration pattern), but their
mtDNA sequences match those of K. spekii, suggesting
hybridization. Additional genetic studies using nuclear
genes are required to verify their putative hybrid status.
However, if there is no evidence for a hybrid identity
in these tortoises, then the morphological characters
thought to be diagnostic for discerning K. spekii and K.
zombensis would be seriously challenged. Moreover,
the characteristic coloration patterns commonly used to
distinguish between Kinixys species tend to fade with
age, rendering older tortoises more or less uniformly
colored (Branch 2008; Broadley 1993; Fig. 2). Hence,
hinge-back tortoises are frequently misidentified. Genetic
verification of specimens which were morphologically
determined by renowned African herpetologists revealed
misidentification rates ranging from 2% for K. zombensis
to 66% for K. natalensis (F. Ihlow and U. Fritz unpub.
November 2019 | Volume 13 | Number 2 | e195
lhlow et al.
Legend
A\ Type specimens
© iNaturalist sightings
e Sightings & records
@ Genetically verified
eet NN
4 7
a ZIMBABWE
‘Cale
al <a
@
500 km
Fig. 1. Known distribution of Kinixys spekii. Range according to TTWG (2017) is displayed as green shaded area. Open circles refer
to iNaturalist observations, while solid green circles represent literature records and specimens deposited in scientific collections.
Solid red circles correspond to genetically verified records, and triangles to name-bearing type specimens of Kinixys spekii and its
synonyms.
data). While older, uniformly colored K. /obatsiana are
mainly confused with K. spekii and vice versa, young
K. spekii are frequently confused with K. natalensis
(Fig. 2). The most reliable morphological trait allowing
distinction between K. natalensis and young K. spekii is
the tricuspid beak of K. natalensis, whereas K. spekii has
a unicuspid beak. Old uniformly colored K. /obatsiana
can be distinguished from K. spekii based on the posterior
Shell rim, which is serrated in K. /obatsiana and smooth
in K. spekii (Fig. 2).
The high misidentification rates show that the
established morphological characters for species
determination are insufficient and call into question the
reliability of published records, photographic vouchers,
Amphib. Reptile Conserv.
and even the identification of specimens (including
name-bearing type specimens) housed in scientific
collections. Given that the putative distribution ranges
(TTWG 2017), which represent an essential tool for
the conservation and management of these species, also
largely rely on collection databases and morphologically
identified individuals, these should be treated with
caution.
To ensure correct species identification of challenging
specimens, molecular genetic verification is strongly
recommended until more robust morphological
characters have been revealed. Photographic vouchers
should include dorsal, ventral, and lateral views to
facilitate accurate species identifications. For K.
November 2019 | Volume 13 | Number 2 | e195
Distribution of Kinixys spekii in Africa
eee
Vey PN Z,
Zee
oe
Fig. 2. Top: Lateral views of adult Kinixys lobatsiana (left) and K.
th OE PME Ny oat Pek tsk all
spekii (right). Center: Ventral views of young (SCL 106 mm)
ta
* Cipla “igh? wel
and adult (SCL 161 mm) K. /obatsiana (left) and young (SCL 131 mm) and adult (SCL 151 mm) K. spekii (right). Note the strongly
serrated posterior marginal scutes in K. /obatsiana compared to the smooth carapace rim in K. spekii. Bottom: Lateral views of adult
K. natalensis (left) and young K. spekii (right). Photos: James Harvey and Flora lhlow.
natalensis additional voucher photographs showing the
tricuspid beak should be taken.
Acknowledgements.—We are grateful to the
following collections, and their curators and managers,
for providing data and photographs of specimens or
access to their collections: Shiela Broadley (National
Museum Zimbabwe), Lauretta Mahlangu (Ditsong
National Museum of Natural History), Garin Cael (Royal
Museum for Central Africa), and José Rosado (Museum of
Comparative Zoology). We further thank Marius Burger
and Steve Spawls, who provided data, pictures, or genetic
samples, and the locals who kindly permitted sampling on
Amphib. Reptile Conserv.
their properties. We are grateful to Anders G.J. Rhodin for
sharing a dataset of occurrence records compiled for the
latest TFTSG checklist. In addition, FI thanks Anja Rauh
and Anke Muller (Senckenberg Dresden) for assistance
during laboratory work. All genetic analyses were done
at the molecular genetic laboratories of the Museum of
Zoology (SGN-SNSD-Mol-Lab), Senckenberg Dresden.
FI profited from a Margarethe Koenig scholarship from
the Zoological Research Museum Alexander Koenig.
In addition, research by FI is supported by the German
Science Foundation (DFG IH 133/1—1). Fieldwork was
partly supported through the Mapula Trust awarded to
MDH.
November 2019 | Volume 13 | Number 2 | e195
lhlow et al.
hitmen Oe
Fig. 3. Top: Lateral views of the putative hybrids from the Afungi Penins
if i P ~ ~ wes § ‘ ~~ =]
@ ~ tS ae
BED f : Ky ;
ula, Cabo Delgado Province, Mozambique, which have
mtDNA sequences of Kinixys spekii but morphologically resemble K. zombensis. Bottom: Lateral views of genetically verified K.
zombensis from KwaZulu-Natal Province, South Africa. Photos: Luke Verburgt and Flora Ihlow.
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species of Kinixys Bell (Reptilia: Testudinidae).
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Provincial Nature Reserves. ‘Transvaal Nature
Conservation Division, Pretoria, South Africa. 38 p.
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P, Vences M, Harvey J, Hauswaldt JS, Schleicher
A, Stuckas H et al. 2012. Molecular phylogeny of
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Testudinidae). Journal of Zoological Systematics and
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O, van der Bank M. 2013. Phylogenetic position
and revised classification of Acacia s.l. (Fabaceae:
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Distribution of Kinixys spekii in Africa
Mimosoideae) in Africa, including new combinations Field Guide to East African Reptiles. Bloomsbury
in Vachellia and Senegalia. Botanical Journal of the Publishing PLC, London, United Kingdom. 624 p.
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Reptiles of the Kruger National Park. National Parks van Dik PP]. 2017. Turtles of the World: Annotated
Board South Africa, Pretoria, South Africa. 236 p. Checklist and Atlas of Taxonomy, Synonymy,
Spawls S, Howell K, Drewes C, Ashe J. 2004. A Field Distribution, and Conservation Status. 8 Edition.
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Spawls S, Howell K, Hinkel H, Menegon M. 2018. USA and Turtle Conservancy, Ojai, California, USA.
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Amphib. Reptile Conserv.
Flora Ihlow is a German herpetologist (Dr. rer. nat.) presently working at the Senckenberg Natural
History Collections, Dresden, Germany. For the past 10 years, Flora’s research has mainly focused
on the herpetofauna of Southeast Asia, in particular on the ecology, systematics, and distribution of
chelonians. She has published numerous scientific papers on these topics. After graduating from the
Rheinische Friedrich-Wilhelms-Universitat (Bonn, Germany), Flora joined the phylogeography group
of Senckenberg Dresden in 2017 as a post doc to study the systematics and distribution of chelonians
from southern Africa. Flora is a member of the IUCN/SSC Tortoise and Freshwater Turtle Specialist
Group (TFTSG).
Harith Farooq has been a Ph.D. student at the University of Aveiro, Portugal, and the University of
Gothenburg, Sweden, since 2016. Harith is supported by the WCS Christensen Conservation Leaders
Scholarship, the World Wildlife Foundation — Education for Nature Scholarship, and the Fundac¢éo
para a Ciéncia e Tecnologia. His main interests are biogeography and conservation, especially in
amphibians and reptiles. Harith has been inventorying these groups across Mozambique since 2011,
resulting in the publication of numerous species descriptions and range extensions. Before embarking
on his Ph.D., Harith worked at the Lurio University, Mozambique, for six years lecturing biological
sciences and publishing articles on science communication and environmental education.
Vaclav Gvozdik is a herpetologist based at the Institute of Vertebrate Biology of the Czech Academy
of Sciences. Vaclav is interested in the phylogeography, diversity, and evolution of amphibians and
reptiles of the Western Palearctic and sub-Saharan Africa. In Africa, he has mostly worked in lowland
and montane rainforests, and in recent years mainly in the rainforests of the Congo Basin. While
Vaclav has been studying various groups of herpetofauna, anurans have been his main focal group.
Margaretha D. Hofmeyr is Professor Emeritus at the Biodiversity and Conservation Biology
Department, University of the Western Cape, South Africa. Margaretha is an ecophysiologist by
training and first studied large ungulates before switching to chelonians. Her ecophysiological studies
revealed that South African tortoises have many unique characteristics, which stimulated her interest
in their genetic diversity and systematics. Margaretha has published extensively on the ecology
and phylogeography of sub-Saharan tortoises and turtles, and she is closely involved in several
conservation projects for threatened tortoises. This work resulted in her being awarded the 2015 Sabin
Turtle Conservation Prize. Margaretha is a member, and Regional Vice-Chair for Africa, of the IUCN/
SSC TFTSG and she coordinated the 2014 and 2018 Red List Assessments for South African tortoises
and freshwater turtles.
Werner Conradie holds a Masters in Environmental Science (M. Env. Sc.) and has 12 years of
experience with the southern African herpetofauna, with his main research interests focusing on the
taxonomy, conservation, and ecology of amphibians and reptiles. Werner has published numerous
principal and collaborative scientific papers, and has served on a number of conservation and
scientific panels, including the Southern African Reptile and Amphibian Relisting Committees. He
has undertaken research expeditions to many African countries including Angola, Botswana, Lesotho,
Malawi, Mozambique, Namibia, South Africa, Zambia, and Zimbabwe. Werner is currently the
Curator of Herpetology at the Port Elizabeth Museum (Bayworld), South Africa.
66 November 2019 | Volume 13 | Number 2 | e195
Amphib. Reptile Conserv.
lhlow et al.
Patrick D. Campbell holds a B.Sc. in Biological Sciences with 33 years working experience in the
department of Life Sciences (Zoology) at the Natural History Museum, London, NHM (UK). Patrick
has travelled the world on official duty as collector, diver, science officer, surveyor, and speaker at
various conferences, as far afield as China, Brazil, Thailand, Kenya, French Guiana, Ecuador, the
United States, Spain, and Milos to name but a few. He has published nearly 50, mostly collaborative,
papers on a variety of topics involving a number of different lower vertebrate species but most recently,
and primarily, on the taxonomy, osteology, and conservation of reptiles. Patrick is currently the Senior
Curator of Reptiles at the NHM (UK).
James Harvey works as an independent herpetologist, ecological researcher, and consultant, living in
South Africa. He holds degrees in Zoology, Hydrology, and Environmental Management, and has 16
years’ experience working with faunal biodiversity. James has performed ecological fieldwork widely,
primarily within Africa, in such countries as South Africa, Botswana, Zimbabwe, Angola, Malawi,
Mozambique, Kenya, Mali, Madagascar, Vietnam, and the Democratic Republic of the Congo. His
interests are diverse but center on the taxonomy, ecology, and conservation of herpetofauna and
other biodiverse groups. James has contributed to conservation assessments, workshops, and Red
Data publications on reptiles, amphibians, mammals, and plants for the southern and eastern African
regions. He regularly attends herpetological conferences, and has published numerous scientific papers
and was a contributing author on many more.
Luke Verburgt is a specialist consulting herpetologist working throughout A frica, with his professional
and scientific research experience extending over 16 years. Luke has published 18 internationally
recognized scientific papers to date on topics including herpetology, evolutionary biology, ecological
physiology, and animal behavior. His professional career covers biodiversity-related work on projects
throughout Africa and its islands (Angola, Botswana, Cameroon, Céte d'Ivoire, Guinea, Lesotho,
Liberia, Madagascar, Malawi, Mali, Marion Island, Mozambique, Namibia, South Africa, Uganda,
and Zimbabwe). Luke currently co-owns and co-directs the Enviro-Insight consultancy (http://www.
enviro-insight.co.za) where he fulfills roles as Director, senior ecological specialist, project manager,
software developer, and GIS specialist.
Uwe Fritz is the head of the Museum of Zoology, Senckenberg Natural History Collections at Dresden,
Germany, and Extraordinary Professor for Zoology at the University of Leipzig, Germany. Uwe has
worked for many years on the taxonomy, systematics, and phylogeography of turtles and tortoises,
and has also studied to a lesser extent snakes and lizards. He is particularly interested in hybridization
patterns and gene flow in contact zones of distinct taxa. Uwe has authored or co-authored numerous
scientific articles, mainly in herpetology, and has also edited various proceedings and books, among
them the two turtle volumes of the Handbook of Amphibians and Reptiles of Europe.
67 November 2019 | Volume 13 | Number 2 | e195
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 68-81 (e197).
Value of forest remnants for montane amphibians on the
livestock grazed Mount Mbam, Cameroon
12.*Arnaud M. Tchassem Fokoua, ‘Legrand Nono Gonwouo, *Joseph L. Tamesse,
and *4Thomas M. Doherty-Bone
‘Laboratory of Zoology, Faculty of Sciences, University of Yaoundé I, P.O. Box 812, Yaoundé, CAMEROON ?*Higher Teacher Training College,
Department of Biological Science, Laboratory of Zoology, Yaoundé, CAMEROON 3?Conservation Programmes, Royal Zoological Society of
Scotland, Edinburgh, UNITED KINGDOM ‘Department of Life Sciences, Natural History Museum, London, UNITED KINGDOM
Abstract.—Habitat loss and degradation are the primary threats to biodiversity, especially for amphibians. In
the Highlands of Cameroon, knowledge on the impacts of different forms of habitat loss, such as livestock
management, is restricted to anecdotal reports. This study investigated the impact of forest fragmentation,
driven primarily by livestock grazing, on the amphibian assemblage on Mount Mbam, West Region, Cameroon.
Stratified, multi-season surveys over two years recorded the abundance and community composition of
anuran species. Based on the revised inventory of amphibians the proportion of threatened species on Mount
Mbam was calculated at 23.52%. A small population of Phrynobatrachus steindachneri was found to occur
despite having completely disappeared on other mountains in its distribution range. One species known to the
mountain, Cardioglossa schioetzi, was not found during the surveys. The remaining forest patches were found
to be significant habitat for several species endemic to the mountains of Cameroon-Nigeria. The savanna,
likely expanded by livestock grazing, held numerous reed frog species that likely benefit from forest loss,
especially in low- to mid-range elevations. The observed relationship between land-use and amphibians on
this mountain indicates that the ongoing conversion of forest to pasture threatens remaining montane endemic
anuran species, with conservation planning and action now necessary.
Keywords. Africa, endemic, frog, grassland, habitat fragmentation, habitat loss
Citation: Tchassem Fokoua AM, Gonwouo LN, Tamesse JL, Doherty-Bone TM. 2019. Value of forest remnants for montane amphibians on the
livestock grazed Mount Mbam, Cameroon. Amphibian & Reptile Conservation 13(2) [Special Section]: 68-81 (e197).
Copyright: © 2019 Tchassem Fokoua et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
[Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 9 March 2019; Accepted: 15 August 2019; Published: 7 November 2019
Introduction
Vertebrate animal taxa are disappearing worldwide at
high rates; especially amphibians, a group which has
a high proportion of threatened species (Stuart et al.
2004; Beebee and Griffiths 2005). The five main factors
believed to be driving global amphibian declines are the
introduction of alien species, habitat alteration, over-
exploitation, global change, and infectious diseases
(Collins and Storfer 2003). The most severe stressor is
physical habitat degradation and destruction (Noss et al.
1997; Stuart et al. 2006). These factors have been found
in combination with enigmatic amphibian declines,
occurring particularly at localities above 400 m asl
in the Americas, Europe, and Australia (Pounds et al.
2006; Vences and Kolher 2008). However, studies on
amphibians in African mountains are limited to a handful
of sites, although recent findings have shown declines
in the Cameroonian mountains that are either enigmatic
(possibly associated with chytridiomycosis) or linked to
Correspondence. * arnaudtchassem@yahoo.fr
Amphib. Reptile Conserv.
habitat loss (Hirschfeld et al. 2016; Tchassem et al., in
press).
Cameroon is one of the most diverse countries in
terms of amphibian species, and it is home to about 4%
of the world’s known species of frogs (IUCN 2017). The
Bamenda Highlands form the northern portion of the
Highlands of Cameroon that includes Mount Mbam. Some
species known to occur in Mount Mbam are only known
from one or a few mountains, including some species
classified as Vulnerable or Endangered in the IUCN Red
List. This mountain has been studied less extensively
than many others, but its study should be a priority given
the community level amphibian declines in neighboring
mountains (Hirschfeld et al. 2016; Tchassem et al., in
press), where the causes remain uncertain as to whether
they are habitat driven or the result to other factors such as
the chtyrid fungus (Batrochochytrium dendrobatidis | Bd).
The impacts of environmental change on the Cameroon
mountains are still unclear, especially regarding habitat
loss, due to limited studies across Sub-Saharan Africa in
November 2019 | Volume 13 | Number 2 | e197
Tchassem Fokoua et al.
general (Buckley and Jetz 2007).
Deforestation rates are exceptionally high across
West and Central Africa (Hansen et al. 2013). In the
biodiverse highlands of Cameroon and Nigeria (Bergl
et al. 2007), forest loss is driven by a combination of
clearance for cultivation, overexploitation of wood
fuel, and incursions by livestock (Chapman et al.
2004). The impact of this loss of forest on amphibians
has so far been assumed to be the loss of montane
endemic species, but the specific factors driving the
declines that are associated with forest loss have
not been determined. This uncertainty includes the
potentially differential impacts of livestock grazing
versus cultivation, for example, with potential
exacerbation by agrochemicals (Tchassem et al.,
in press). This scenario is especially applicable to
the degradation of natural habitats in the Bamenda
Highlands of Cameroon, that include Mounts Oku,
Bamboutos, Lefo, and Mbam, which share similar
montane endemic species (Cheek et al. 2000; Doherty-
Bone and Gvozdik 2017). Montane forest cover
has decreased dramatically during the 20" and 21
centuries; with remaining forests becoming highly
fragmented (Abbot et al. 2001; Doherty-Bone and
Gvozdik 2017). Agrochemical pollution and grazing
have not been systematically studied in this area, and
since they often occur simultaneously, differentiating
the impacts of each stressor is difficult (Tchassem et
al., In press).
Mount Mbam has historically been appraised for
amphibian diversity, with several montane endemic
species identified in the 1970s, such as Perret’s Egg Frog
(Leptodatylodon perreti) and Steindachner’s Puddle
Frog (Phrynobatrachus steindachneri) [Amiet 1971,
1973, 1976]. Despite this work, the mountain has no
official protection, and deforestation remains unchecked.
Unlike other mountains in the Bamenda Highlands,
Mount Mbam does not have considerable cultivation of
crops in contrast to its widespread livestock grazing. This
study focuses on Mount Mbam to assess the status of the
amphibian community and threats from encroachment
by livestock grazing. Grazed areas and remnant forests
were surveyed, incorporating an elevational gradient,
to determine: (1) whether the diversity of amphibians
has been altered compared to historical records; and (2)
which amphibian species are excluded from the grazed
areas compared to the gallery forest.
Materials and Methods
Study area. Mount Mbam (sometimes known as the
Mbam Hill Forest), is a calcareous massif located near the
town of Foumban in the West Region of Cameroon (Fig.
1, 05°57°N, 10°44’E). It rises from the savanna plains
at 1,000 m to a summit of 2,100 m asl. The vegetation
of the mountain 1s transitional between montane savanna
grassland mixed with patches of gallery forest (Fotso
Amphib. Reptile Conserv.
et al. 2001; Fig. 2). The forest patches are dominated
by Albizia gummifera, Polyscias fulva, and Schefflera
mannii (Fotso et al. 2001). Human communities living
around and using the mountain include the Banso’o,
Haoussa, and Fulani peoples. Livestock grazing is
predominately practiced by the Fulani community, who
are semi-nomadic, and concentrated at higher elevations
where they live for nine months during the year, from
April to December. During January to March (the dry
season), these cattle herders move down the mountain to
other pastures at lower altitudes.
Study design. To ensure a representative appraisal
of diversity, the Mount Mbam amphibian fauna was
surveyed over a period of two years, between 2014 and
2016. Field surveys were deployed, with all sample
sites visited at least three times. During diurnal and
nocturnal visual encounter surveys (VES) with a total
duration of 96 surveyor-hours across each land use type
were used to quantitatively sample fossorial, arboreal,
and water-associated amphibian species (Rodel and
Ernst 2004). Nocturnal acoustic encounter surveys were
also used to detect animals. Opportunistic sampling
was made for all taxa throughout the survey to enable
additions to the updated inventory. All sampling sites
were characterized with the following environmental
data: altitude and coordinates (recorded with a Garmin®
GPS exter 90), presence of potential breeding sites,
regime of disturbance, and vegetation structure. The
vegetation was determined at three strata (canopy cover,
shrubs, and understory). Surveys were stratified between
gallery forest (the only remnant forest on the mountain)
and grassland (primarily grazed by livestock). Surveys
involved searching of microhabitats, such as lifting rocks
and logs, peeling away bark from trees, moving fallen
debris, and inspecting tree stems during daytime (07:00-
12:00 h) and night time (19:00—00:00 h) along streams,
ponds, and the surrounding vegetation (Crump and Scott
1994; Rodel and Ernst 2004). Amphibians were captured
by hand, and then identified and released where they
were found. However, a subset of 1-3 individuals of
each species, and specimens difficult to identify in the
field, were euthanized using an overdose of MS-222 or
chlorobutanol solution and preserved in 75% ethanol.
These specimens have been deposited in the University
of Yaoundé I, Laboratory of Zoology. For species
identification, original descriptions and derived literature
were used (Perret 1966; Amiet 1977, 1980, 2012: Schiotz
1999).
Data Analysis. The proportion of threatened species
in the total amphibian species inventory for Mount
Mbam (both historical and contemporary species
observed) was calculated following Bohm et al. (2013).
All other analyses were performed with the statistical
package R version 3.3.2 (R Core Team 2016). Inventory
completeness was assessed using an incidence-based
November 2019 | Volume 13 | Number 2 | e197
Amphibians of Mount Mbam, Cameroon
a Ny ' } Le*
ty 1
jo —_ Summit iF
Ll 4S
q : if } RM nal .
i Wh j = c~\\ =
rn | ®) | oe wy
ag a ALA a
i | VJ it |
Li a
1 | | hy |
tr | 1
} 4 ry
i |e
| } a 6f i N
| J | .
| af | und i
| i
1.5 Km
a j* \ 7 7
fod -_ A Pasture
kJ 7
} 4 Swap area
e if
ig ae @ Forest patches
a8 a
@ Settlement
Fig. 1. Maps showing (top) the topography of the Bamenda Highlands, white circle showing Mount Mbam in the West Region of
Cameroon; and (bottom) the layout of sample sites on Mount Mbam.
estimator with the package BiodiversityR (Colwell and
Coddington 1994). To compare the amphibian community
composition between habitat types, PERMANOVA
analysis (formula: Adonis, library: vegan) was used to
test the significance of the Bray-Curtis dissimilarity
based on 999 permutations (Anderson 2001; Riemann
et al. 2017). Amphibian abundance data transformed
by square root were subjected to ordination analysis
using non-metric scale (NMDS) plots of Bray-Curtis
dissimilarity (formula: metaMDS, library: vegan) to view
the dispersion of similarities. The species contribution
to differences between different types of habitats was
evaluated by SIMPER analysis (Clarke 1993). The
influence of habitat (forest patches, pasture-grassland)
on species abundance was evaluated using Generalized
Linear Models (GLM, formula: glm, data family:
Amphib. Reptile Conserv.
70
poisson) [O’Hara and Kotze 2010]. Various parameters
such as season, year, and elevation were incorporated
into the GLMs to assess potential confounding factors
against the response variables (abundance of frogs).
GLMs were restricted to species for which a minimum
of five individuals were recorded in the surveys.
Information criterion analysis was then applied to the
GLMs, in which derived Akaike’s Information Criteria
were used to assess the best performing model based on
incorporation of these potentially competing explanatory
factors (Mazerolle 2006).
Results
The surveys revealed 17 anuran species of seven genera
among 225 individuals (Table 2). Based on these and
November 2019 | Volume 13 | Number 2 | e197
Tchassem Fokoua et al.
Bech nth es Ed re ae RR a 2 game a’ ae
Fig. 2. Montane habitats of amphibian species observed in recent surveys of Mount Mbam, West-Region, Cameroon: a) gallery
forest during the rainy season; b): gallery forest during the dry season after a bushfire; c) savanna area transformed by overgrazing;
and d): effects of bushfire started for pasture on the same site during the dry season.
iS
=r
historical records, the proportion of threatened species ==rheophilus, which shared the same breeding sites
on Mount Mbam is estimated at 23.52%. However, the (streams) [Table 3]. Leptopelis notatus was more
species accumulation curve over the survey periods did dominant in forests at lower elevations (1,307—1,340 m).
show a plateau, indicating the discovery of more species The only anurans of Phryobatrachidae on the mountain
with further searching is unlikely (Fig. 3). In comparison — were P. steindachneri restricted to forests at 1,400—1,800
to historical records, one species missing from the m (Tables 2—3). The only Hyperoliidae found in the
contemporary surveys was Cardioglossa schioetzi (Table forests were a singleton of Afrixalus aff. fulvovittatus (at
1). The Puddle Frog, Phrynobatrachus steindachneri, 1,342 m) and two individuals of Hyperolius ighettensis
was found, but only four sub-adult individuals were (at 1,342—1,684 m), though they likely spilled over from
observed over the two years. Species new to the historical the grassland areas.
inventory included the Rocket Frog Ptychadena Within derived savanna (i.e., savanna created by cattle
mascareniensis “D” (Zimkus et al. 2016) andthe Clawed grazing and fire) Hyperoliidae (43.55% of all individual
Frog Xenopus cf. eysoole (Fig. 4m). The latter species frogs) was the most dominant group, represented
was found as high as 1,600 m asl in stagnant water bodies — primarily below 1,500 m by HAyperolius concolor, H.
(including wells) that were heavily frequented by local balfouri, H. tuberculatus, H. igbettensis, H. nitidulus, H.
people and livestock. cinnamomeoventris, and A. aff. fulvovittatus (Tables 2-3).
Community structure (measured by Bray-Curtis — This family was followed by Pipidae (25.8% of individuals,
dissimilarity) between the two habitat types was _ represented by X. cf. eysoole only), Arthroleptidae (7%
significantly different (PERMANOVA: p = 0.01, Fig. — for LZ. notatus, L. nordequatorialis, as well as a minority
5). Most amphibian species were found in savanna (13 _ of five individual A. montanus), Ptychadenidae (5.8%,
species, 76.47% of individual frogs), with seven species represented by P mascareniensis “D” only), Bufonidae
(16% of individuals) found in forest (Table 2). Gallery = (2.2% for Sclerophrys maculata only), and Dicroglossidae
forests were dominated by species of Arthroleptidae, (2.2% for Hoplobatrachus occipitalis only). Four species
notably Astylosternus montanus, L. perreti, and A. occurred in both habitats: A. aff. fulvovittatus, A. montanus,
Amphib. Reptile Conserv. 71 November 2019 | Volume 13 | Number 2 | e197
Amphibians of Mount Mbam, Cameroon
Table 1. An updated amphibian species inventory for Mount Mbam, Cameroon.
Anuran taxa
Arthroleptidae
Astylosternus montanus Amiet, 1978
Astylosternus rheophilus Amiet, 1977
Cardioglossa schioetzi Amiet, 1982
Leptodactylodon perreti Amiet, 1971
Leptopelis nordequatorialis Perret, 1966
Leptopelis notatus (Peters, 1875)
Bufonidae
Sclerophrys maculata (Hallowell, 1854)
Hoplobatrachus occipitalis Gunther, 1858
Hyperolidae
Afrixalus aff. fulvovittatus Pickersgill, 2007
Hyperolius balfouri Werner, 1907
Hyperolius cf. cinnamomeoventris Bocage, 1866
Hyperolius igbettensis Mertens, 1940
Peters, 1875
Mocquard, 1897
Hyperolius nitidulus
Hyperolius tuberculatus
Pipidae
Xenopus cf. eysoole Evans et al. 2015
Phrynobatrachidae
Phrynobatrachus steindachneri Neiden, 1910
Ptychadenidae
Ptychadena mascareniensis “D” Zimkus et al. 2017
Species authority Global IUCN status
Le
VU
VU
EN
LC
LC
LC
Le
EC;
LC
LC
Le
LC
Le.
VU
LC
Endemicity References
CNH Amiet 1978; present study
CNH Amiet 1977; Hirschfeld et al. 2016; present
study
CNH Amiet 1982; Schietz 2004
BamH Amiet 1980; present study
CNH Perret 1966; Amiet 1971, 1974, 1980;
Gartshore 1986; present study
S-Sa Boulenger 1906; Nieden 1909; Goin 1961;
present study
PanAfr Hirschfeld et al. 2016; present study
S-Sa present study
S-Sa Perret 1976; present study
S-Sa Werner 1908; Scortecci 1943; Monard,
1951; present study
S-Sa Inger 1968; Largen and Dowsett-Lemaire
1991; Schiotz 1999; present study
S-Sa Schiotz 1963; present study
S-Sa Perret 1966; present study
S-Sa present study
present study
CNH Mertens 1968; Hirschfeld et al. 2016
S-Sa present study
Endemicity codes for species limited to: S-Sa - sub-Saharan Africa; C.W.A+Ng - Central and West African countries and Nigeria; BamH — just
the Bamenda Highlands of Cameroon that includes Mount Mbam; CNH: just the Bamenda Highlands of Cameroon and Nigeria.
H. igbettensis, and L. notatus.
Species represented by at least five individuals,
regardless of habitat type, varied with the strength of
the models in relation to habitat type. Species usually
associated with forest had better fitted models with
habitat (AAIC 0-7) and significant p-values, notably
Astylosternus sp. and L. perreti, as well as some savanna
species such as P. mascariensis “D,” H. nititdulus, and H.
tuberculatus (Table 4). Species associated with savanna
(Afrixalus, some Hyperolius sp., and S. maculata) and L.
notatus, however, did not show statistically significant or
well fitted models with habitat as a fixed variable (Table
4). Habitat* elevation and season* elevation both provided
the best fitted models (the lowest AIC) for A. rheophilus,
with a AAIC of seven from the inclusion of habitat
alone or from the inclusion of habitat*elevation* season.
Habitat is a major contributor for the best fitted
models for the species A. montanus (habitat*year), L.
notatus (habitat*elevation), and P mascareniensis “D”
(habitat*season) [Table 4]. Year of survey did have an
influence over the fit of the models, with the exceptions
of H. cinnamomeoventris, P. mascareniensis, and S.
Amphib. Reptile Conserv.
72
maculata, manifest by all three having fewer records for
the year 2016. For the remaining species, the lack of an
influence of year indicates population stability in this
two-year time period on the mountain.
Discussion
This study quantitatively assessed the status and habitat
use of amphibians on Mount Mbam, Cameroon, in rela-
tion to land use. The species inventory of the amphibians
of the mountain was updated, revealing little additional
diversity recorded for the Mbam massif so far, beyond
more lowland-adapted species. The stratified survey en-
abled better understanding of the habitat requirements of
numerous amphibian species, especially montane species
with restricted ranges. Species composition varied con-
siderably between montane savanna and forest habitats.
With a higher elevation, the forest was generally found
to have fewer species, but with considerably more nu-
merous montane endemic species. There were clear 1n-
stances of spillover from one habitat to another, typified
by the occurrences of a minority of species in one habitat
compared to the habitat in which they are numerically
November 2019 | Volume 13 | Number 2 | e197
Tchassem Fokoua et al.
A
ot
.
Number of species
oo
30 40
30
pecee eens see e ee ee EPO P EERE EEE ED
eeaseeeea ear eeee
saee
weeeet
eet
eaaaee
anor
wat
aenet
ate
Savanna
— Forest
60 70 80 90 100
Samples
Fig. 3. Species accumulation curves of Mount Mbam by land use based on contemporary records.
dominant.
Compared to nearby mountains such as Oku
or Bamboutos, Mount Mbam has a more diverse
community of hyperoliids, likely due to a greater area
of the mountain consisting of lower elevations. This
is in contrast to mountains such as Bamboutos, where
agrochemicals are widely used. It is notable that the
genera Arthroleptis and Kassina were not observed
in either historical or contemporary surveys, and the
explanation for their absence is unclear. Montane
endemic species known to Mounts Lefo, Oku, and
Bamboutos, including Cardioglossa oreas, C. pulchra,
and Astylosternus ranoides, were not found on Mbam.
This is despite other species such as Leptodactylodon
perreti and A. rheophilus occurring on this mountain,
and the fact that these absent species do have elevational
ranges corresponding to that of Mt. Mbam. This suggests
the possibilities that they are either: (1) locally extinct
through human land use practices or climate change that
pre-date the first surveys of the mountain in the 1960s, or
(ii) that the mountain is too small and low in elevation for
viable populations of the higher montane endemic frog
species to persist.
Despite its disappearances on Mount Oku in the
North West Region and Mount Bamboutos in the West
Region (Doherty-Bone and Gvozdik 2017; Tchassem
et al., in press), P steindachneri was observed during
the recent field surveys. This taxon is part of a species
complex that could possibly also include P. jimzimkusi
(Zimkus and Gvozdik 2013). Cardioglossa_ schioetzi
was not observed in this study, and it was also not found
on Mount Oku in recent years, as with certain other
species of Cardioglossa, Werneria, and Phrynobatrachus
(Hirschfeld et al. 2016; Doherty-Bone and GvoZzdik
2017; Tchassem et al., in press). The causes of these
disappearances remain unknown, but the declines on
Mount Manengouba and Mount Oku have coincided
with an increase in the prevalence of amphibian chytrid
fungus (Batrachochytrium dendrobatidis, Bd), indicating
that disease could be a factor (Hirschfeld et al. 2016).
Amphib. Reptile Conserv.
73
The role of climate change in these declines also remains
unclear and represents a research gap that requires urgent
attention (Doherty-Bone and GvoZdik 2017; Tchassem et
al., in press). On Mount Mbam, further research should
include investigating the role of fire, which could be
a factor, not just from its use by livestock herders but
Table 2. Summary of amphibian species (total per habitat type
across all survey techniques) encountered during the present
study (2014—2016).
Pasture-
grassland
Afrixalus aff. fulvovittatus Pe 1
Gallery
Species forest
—
&
Astylosternus montanus
Astylosternus rheophilus
Hoplobatrachus occipitalis
Hyperolius balfouri
Hyperolius tuberculatus
Hyperolius concolor
Hyperolius igbettensis Gi
Hyperolius nitidulus
Hyperolius cinnamomeoventris 7
Leptodactylodon perreti 5
Leptopelis nordequatorialis 2
8
Leptopelis notatus
Phrynobatrachus steindachneri
1
5
2
La
Sclerophrys maculata f tl
Ptychadena mascareniensis “D” 13:
Xenopus cf. eysoole 8
189
23.63
November 2019 | Volume 13 | Number 2 | e197
Total 3
2
5
4
5
Ls 0
Dee Se
Species richness 7
0.80
2.44
4.50
Species evenness
Shannon’s D
Mean number of specimens per sampling
event
Amphibians of Mount Mbam, Cameroon
' Y= | a a : ie
Fig. 4. Montane endemic amphibian species observed in recent surveys of Mount Mbam, West-Region, Cameroon. a) Astylosternus
rheophilus, b) Astylosternus montanus, ¢) Afrixalus aff. fulvovittatus, d) Hyperolius balfouri, e) Hyperolius igbettensis, f)
Hyperolius nitidulus, g) Hyperolius concolor, h) Hyperolius cinnamomeoventris, i) Hyperolius tuberculatus, j) Leptopelis
nordequatorialis, k) Leptopelis boulengeri, 1) Phrynobatrachus steindachneri, m) Xenopus cf. eysoole, n) Hoplobatrachus
occipitalis, and 0) Sclerophrys maculata.
Amphib. Reptile Conserv. 74 November 2019 | Volume 13 | Number 2 | e197
Tchassem Fokoua et al.
Stress = 0.00005
Permanova: p<0,01
NMDS2
(e)
Savanna Area
Forest patches
-2
-4
-5 0 5
NMDS1
Fig. 5. Non-metric dimensional scaling plot of amphibian
community structure divided by land use type on Mount Mbam
based on visual encounter surveys with equal effort for each land
use. The PERMANOVA p-value is shown in the top right corner.
also its influence by climate change. Some species were
possibly overlooked during this study, possibly due to
variance in the detectability of rare and/or cryptic species
(Mackenzie et al. 2005; Megson et al. 2009); thus,
further efforts to continue this study would benefit from
complementary survey methods such as pitfall traps and
continuous audio recordings. However, it is also possible
that the species pool for Mount Mbam has simply been
degraded historically.
The presence of livestock grazing on the slopes of
Mount Mbam has likely modified the landscape structure
of habitats to a great extent, such as through loss of
forest from grazing, fires, and trampling by livestock
(Carte and John 2002). The remaining forest on Mount
Mbam is now reduced to patches along streams and close
to the summit where access is difficult for livestock.
The historical loss of forest is likely to have negatively
affected populations of forest-dependent species, while
potentially benefitting tolerant, savanna-adapted species.
While the forests hosted fewer species than savanna,
those species are montane endemics of conservation
concern, while the greater species richness of the savanna
consists of species with broader, lowland ranges. Most of
the amphibian species were significantly influenced by
elevation, habitat, and season. This indicates that despite
more savanna becoming available, the colonization by
lowland species may remain limited.
Planning and implementing effective strategies to
control habitat disturbance and encourage recovery
on this mountain could be required to stop further loss
of montane endemic species in the long term. Future
studies should investigate the precise impacts of bushfire,
including influences on nutrient cycling, water quality,
predation risk to anurans, and reproductive success. The
conservation needs of Mount Mbam are similar to those
of Mount Bamboutos, but are driven more by livestock
than the cultivation of crops. As with Mount Bamboutos,
Mount Mbam has neither official protection nor
conservation action, and the exploitation of its resources
is unregulated. Several measures could be implemented
to reduce the rate of forest loss on Mount Mbam. Steps
such as raising environmental awareness, conducting
educational seminars, and preparing educational
materials for the locals, would certainly have a positive
Table 3. Similarity percentage (SIMPER) analysis showing importance of dissimilarity for various amphibian species for habitat
type based on visual encounter surveys of Mount Mbam.
Mean number of individuals per survey
Taxon Forest Pasture-grassland eet mes te wana
Xenopus cf. eysoole 0+0 0.64 + 1.24 0.17 0.17
Astylosternus montanus 0.47 + 0.86 0.06 + 0.23 0.14 0.32
Leptopelis notatus 0.17+0.42 0.07 + 0.39 0.08 0.39
Hyperolius balfouri 0+0 0.23 + 0.75 0.07 0.46
FHyperolius concolor 0+0 0.24 + 0.96 0.06 0.58
Afrixalus aff. fulvovittatus 0.03 + 0.18 0.17 + 0.60 0.06 0.52
Astylosternus rheophilus 0.17+ 0.46 0+0 0.05 0.69
Hyperolius igbettensis 0.07 + 0.25 0.08 + 0.37 0.05 0.79
Hyperolius tuberculatus 0+0 0.17 + 0.64 0.05 0.89
Phrynobatrachus steindachneri 0.13 + 0.35 0+0 0.05 0.84
Ptychadena mascareniensis 0+0 0.14+0.49 0.05 0.63
FHyperolius cinnamomeoventris 0+0 0.08 + 0.37 0.03 0.95
Hyperolius nitidulus 0+0 0.09 + 0.41 0.03 0.92
Sclerophrys maculata 0+0 0.06 + 0.23 0.03 0.97
Hoplobatrachus occipitalis 0+0 0.06 + 0.38 0.02 0.99
Leptopelis nordequatorialis 0+0 0.02 + 0.15 0.01 1
Amphib. Reptile Conserv. 75 November 2019 | Volume 13 | Number 2 | e197
Amphibians of Mount Mbam, Cameroon
Table 4. Generalized linear models comparing parameters which influence the abundance of amphibian species on Mount Mbam.
Species
Afrixalus aff. fulvovittatus
Astylosternus montanus
Astylosternus rheophilus
Hoplobatrachus occipitalis
Hyperolius balfouri
Amphib. Reptile Conserv.
Model parameters
Habitat* Elevation* Season
Habitat* Elevation
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
Season
Year
Habitat* Elevation* Season
Habitat* Elevation
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
Season
Year
Habitat* Elevation* Season
Habitat* Elevation
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
Season
Year
Habitat* Elevation* Season
Habitat* Elevation
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
Season
Year
Habitat* Elevation* Season
Habitat* Elevation
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
76
df
112
116
116
116
116
118
118
118
KZ
112
116
116
116
116
118
118
118
118
112
116
116
116
116
118
118
118
118
112
116
116
116
116
118
118
118
118
112
116
116
116
116
118
118
Residual
deviance
41.48
63552
62.95
47.88
77.78
84.83
74.05
81.87
88.35
51.96
a9: 92
56.69
64.91
53.47
64.11
TT9
68.49
81.52
9.76
9.76
20.00
992
20.51
20.69
9:93
30.50
31.11
34.40
35.47
38.26
34.65
29.11
38.268
35.64
41.05
204.44
68.50
90.26
76.22
69.92
99.10
99.26
OV 2
November 2019 | Volume 13 | Number 2 | e197
p-value
0.99
<0.01
<0.001
<0.001
0.01
0.05
<0.001
<0.01
0.53
0.99
0.06
0.99
0.99
0.90
<0.001
<0.01
<0.001
0.12
AIC
78
269.90
108
123
108
102
131
128
119
AAIC
Tchassem Fokoua et al.
Table 4 (Cont.). Generalized linear models comparing parameters which influence the abundance of amphibian species on Mount Mbam.
Species Model parameters df ae p-value AIC AAIC
Season 118 94.31 <0.001 123 21
Year 118 111.34 0.94 139 36
Hyperolius cinnamomeoventris _ Habitat*Elevation* Season 112 39.44 1.00 65 19
Habitat* Elevation 116 42.10 0.99 60 14
Habitat* Season 116 44.07 1.00 62 16
Season* Elevation 116 40.14 0.13 58 12
Habitat* Year 116 31.24 1.00 49 3
Habitat 118 44.07 0.04 58 12
Elevation 118 42.49 0.02 56 10
Season 118 47.83 0.60 62 16
Year 118 32.36 <0.001 46 0)
Hyperolius concolor Habitat* Elevation* Season 112 82.19 0.99 119 0
Habitat* Elevation 116 103.88 0.99 132 13
Habitat* Season 116 108.83 0.99 137 19
Season* Elevation 116 100.95 <0.001 129 10
Habitat* Year 116 116.84 0.99 145 26
Habitat 118 11732. <0.001 142 2
Elevation 118 129.98 0.97 154 35
Season 118 125.50 0.03 150 31
Year 118 129.81 0.68 154 ae
Hyperolius igbettensis Habitat* Elevation* Season 112 044.07 0.19 74 2
Habitat* Elevation 116 53.05 0.36 7 3
Habitat* Season 116 52.12 0.13 74 2
Season* Elevation 116 53.54 0.46 75 3
Habitat* Year 116 54.83 0.81 76 4
Habitat 118 54.91 0.84 73 1
Elevation 118 54.30 0.42 72 0)
Season 118 54.46 0.49 Te. 0)
Year 118 54.93 0.91 73 1
Hyperolius nitidulus Habitat* Elevation* Season 112 43.35 1.00 71 i
Habitat* Elevation 116 48.10 0.99 68 4
Habitat* Season 116 4471 1.00 64 0
Season* Elevation 116 46.39 0.30 66 2
Habitat* Year 116 46.23 0.99 65 1
Habitat 118 48.10 0.03 64 0)
Elevation 118 50.29 0x12. 66 2
Season 118 50.85 0.17 66 3
Year 118 49.48 0.07 65 1
Hyperolius tuberculatus Habitat* Elevation* Season 112 73.36 0.99 106 7
Habitat* Elevation 116 79.67 0.99 104 >
Habitat* Season 116 75.91 0.99 100 1
Season* Elevation 116 74.91 0.33 99 0
Habitat* Year 116 81.60 0.99 106 7
Amphib. Reptile Conserv. 77 November 2019 | Volume 13 | Number 2 | e197
Amphibians of Mount Mbam, Cameroon
Table 4 (Cont.). Generalized linear models comparing parameters which influence the abundance of amphibian species on Mount Mbam.
Residual
Species Model parameters df aur ate p-value AIC AAIC
Habitat 118 81.85 <0. O1 103 4
Elevation 118 80.99 <0.01 101 2
Season 118 87.32 <0. O1 108
Year 118 90.41 0.79 111 | ie.
Leptodactylodon perreti Habitat* Elevation* Season 112 14.52 0.99 39 1]
Habitat* Elevation 116 14.54 0.99 31 3
Habitat* Season 116 20.00 1.00 aE 9
Season* Elevation 116 14.99 0.99 32 4
Habitat* Year 116 20.51 0.99 Bd 9
Habitat 118 20.69 <0.001 33 5
Elevation 118 15.07 <0.001 28 0)
Season 118 30.49 0.04 43 15
Year 118 34.12 0.51 46 18
Leptopelis notatus Habitat* Elevation* Season 112 31.79 0.99 65 14
Habitat* Elevation 116 43.04 <0.01 69 0
Habitat* Season 116 48.74 0.01 74 5
Season* Elevation 116 48.84 <0.01 74 5
Habitat* Year 116 58.95 0.85 84 14
Habitat 118 59.78 0.14 81 12
Elevation 118 61.16 0.38 83 12
Season 118 59.86 0.15 81 12
Year 118 60.98 0.33 82 13
Ptychadena mascareniensis “D” Habitat* Elevation* Season 112 52.10 1.00 88 4
Habitat* Elevation 116 61.89 0.99 90 6
Habitat* Season 116 55.95 0.99 84 0)
Season* Elevation 116 58.16 0.28 86 2
Habitat* Year 116 57.98 0.99 86 2
Habitat 118 62.44 <0.01 87 3
Elevation 118 67.71 0.14 90 6
Season 118 59.56 <0.01 84 0
Year 118 156 <0.001 90 6
Sclerophrys maculata Habitat* Elevation* Season 112 27.81 1.00 54 20
Habitat* Elevation 116 28.90 1.00 5] 23
Habitat* Season 116 28.27 0.99 46 12
Season* Elevation 116 28.49 0.33 46 12
Habitat* Year 116 19.74 0.99 38
Habitat 118 28.90 0.09 43
Elevation 118 30.34 0.23 44 10
Season 118 30.30 0.22 44 10
Year 118 20.54 <0.001 34 0
Xenopus cf. eysoole Habitat* Elevation* Season* Year -] 0 1.00 148 103
Habitat* Elevation* Season 112 151.00 1.00 228 183
Habitat* Elevation 116 172.00 0.99 241 196
Amphib. Reptile Conserv. 78 November 2019 | Volume 13 | Number 2 | e197
Tchassem Fokoua et al.
Table 4 (Cont.). Generalized linear models comparing parameters which influence the abundance of amphibian species on Mount Mbam.
Species Model parameters
Habitat* Season
Season* Elevation
Habitat* Year
Habitat
Elevation
Season
Year
effect on changing negative attitudes. The creation of a
protected area for these habitats, with strong involvement
of the local people, would be a plausible strategy. The
proportion of endangered species of the Mount Mbam
is very low, but this does not in any way diminish
its importance for the conservation of the endemic
amphibian species, whereas the differences observed at
low and high altitudes with regard to species composition
and habitat type should make this site a national or sub-
regional conservation priority.
Acknowledgments.—The authors express their gratitude
to the Cameroon Ministry of Scientific Research and
Innovation and the Ministry of Forestry and Wildlife
for authorizing our fieldwork (permit number 629PRS/
MINFOF/SG/DFAP/SDVEEF/SC). We especially thank
Mark Wilkinson, Natural History Museum, London,
United Kingdom for assistance. We thank the Rufford
Small Grant (RSG) for funding this work. In addition, we
wish to acknowledge the village chiefs and community
elders who permitted the work on their land, and thank
field assistants Mballa Moussa and Daho. The authors
also thank the reviewers for helping to improve this
manuscript.
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Amphib. Reptile Conserv.
Tchassem Fokoua et al.
Arnaud Marius Tchassem Fokoua is currently a third year Ph.D. candidate at the University
of Yaoundé I, Cameroon. Arnaud received his Bachelor’s degree at the same university,
completing multiple research projects in the domain of herpetology. His research focuses
on the community ecology and conservation of African amphibians, especially aiming
to understand how altitude and anthropogenic activities influence amphibian community
composition.
Legrand Gonwouo Nono (Ph.D.) is a conservation herpetologist from University of Yaoundé
I with experience in central African reptiles and amphibians. Dr. Gonwouo Nono has long-
term experience studying the amphibians and reptiles of Cameroon, particularly in the fields
of biodiversity, taxonomy, and ecology. His recent research interest focuses on the responses
of biodiversity to environmental change, with particular interest in the distributions and
dynamics of endemic species near their geographic range margins.
Joseph Lebel Tamesse is a professor at the Higher Teacher Training College in Cameroon.
Joseph Lebel has a great deal of experience in the study of the psyllids of Cameroon,
particularly in the fields of biodiversity, taxonomy, and ecology. His current studies integrate
multiple fields, and he also supervises several Ph.D. students with research which focuses
on the ecology of millipedes, amphibians, and freshwater crabs. He has co-authored over 50
scientific papers.
Thomas Doherty-Bone is an ecologist researching conservation biology, management, and
herpetology. Thomas is associated with the Royal Zoological Society of Scotland and the
Natural History Museum, London, and holds a Ph.D. in freshwater ecology and invasive alien
species from the University of Leeds, United Kingdom. His research has focused specifically
on montane amphibian ecology and conservation in Cameroon for over 12 years, including
the occurrence of amphibian chytrid fungus and the conservation of Lake Oku and its endemic
clawed frog (Xenopus longipes).
81 November 2019 | Volume 13 | Number 2 | e197
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 82-95 (e199).
urn:lsid:zoobank.org:pub:63D950B1-10B3-4EC1-B4E6-8558F5618DF6
Another Angolan Namib endemic species: a new
Nucras Gray, 1838 (Squamata: Lacertidae) from
south-western Angola
12William R. Branch, ***Werner Conradie, *°°Pedro Vaz Pinto, and ’*Krystal A. Tolley
'Port Elizabeth Museum, P.O. Box 13147, Humewood, Port Elizabeth 6013, SOUTH AFRICA *Department of Zoology, Nelson Mandela University,
Port Elizabeth 6031, SOUTH AFRICA °?School of Natural Resource Management, George Campus, Nelson Mandela University, George 6530,
SOUTH AFRICA ‘Fundagao Kissama, Rua 60 Casa 560, Lar do Patriota, Luanda, ANGOLA °CIBIO/InMBIO, Centro de Investigagdo em
Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairdo, Vairdo, PORTUGAL °TwinLab CIBIO/ISCED, Instituto Superior
de Ciéncias da Educagdo da Huila, Rua Sarmento Rodrigues s/n, Lubango, ANGOLA ‘South African National Biodiversity Institute, Kirstenbosch
Research Centre, Private Bag X7, Claremont 7735, Cape Town, SOUTH AFRICA *Centre for Ecological Genomics and Wildlife Conservation,
Department of Zoology, University of Johannesburg, Auckland Park, 2000, Johannesburg, SOUTH AFRICA
Abstract—A new endemic Sandveld Lizard, genus Nucras, is described from south-western Angola.
Morphologically it resembles members of the Nucras tessellata group, but it is genetically separated and is sister
to the larger tessellata + lalandii group. Although the genus is generally very conservative morphologically,
the new species differs from other congeners in a combination of scalation, overall dorsal color pattern, and
geographic separation. The new species is known from fewer than 12 specimens collected over a period
spanning 120 years from arid south-western Angola. This brings the total number of species in the genus
to 12 and adds another species to the growing list of endemic species of the Namib region of Angola. This
new finding further reinforces the idea that this Kaokoveld Desert region is a key biodiversity area worthy of
conservation and long-term protection.
Keywords. Sandveld Lizard, taxonomy, Africa, endemism, Kaokoveld, biodiversity hotspot
Citation: Branch WR, Conradie W, Vaz Pinto P, Tolley KA. 2019. Another Angolan Namib endemic species: a new Nucras Gray, 1838 (Squamata:
Lacertidae) from south-western Angola. Amphibian & Reptile Conservation 13(2) [Special Section]: 82-95 (e199).
Copyright: © 2019 Branch et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 8 May 2019; Accepted: 8 August 2019; Published: 8 November 2019
Introduction At present, the family Lacertidae is represented in
Angola by 13 species in six genera; Heliobolus (one
species), Holaspis (one), Ichnotropis (three), Meroles
(three), Nucras (two), and Pedioplanis (three; see Marques
The recorded reptile diversity in Angola (278 species,
Marques et al. 2018; Branch et al. 2019) is significantly
lower than that of South Africa (407 species, Tolley et al.
2019), a nearby country of comparable size and habitat
diversity. This incongruity has been attributed to the lack of
recent faunal surveys and/or taxonomic revision of groups
in the country (Marques et al. 2018; Branch et al. 2019).
That this gap simply represents under-sampling of the
Angolan herpetofauna is evidenced by the recent discovery
of numerous new species, including lacertids of genus
Pedioplanis (Conradie et al. 2012), girdled lizards of genus
Cordylus (Stanley et al. 2016; Marques et al. 2019b), and a
new skink of genus Trachylepis (Marques et al. 2019a), as
well as several candidate new species of lacertids (Branch
and Tolley 2017), and geckos (Branch et al. 2017).
Correspondence. * werner@bayworld.co.za
Amphib. Reptile Conserv.
et al. 2018; Branch et al. 2019). The lacertid generic
diversity is comparable to that of other herpetologically
rich areas in sub-Saharan Africa, e.g., eight genera in
Tanzania, Kenya, and South Africa, and five in Namibia
(Branch 1998; Spawls et al. 2018). However, the lacertid
species diversity in Angola (13 species) is notably lower:
Kenya (15), Tanzania (16), Namibia (25), and South
Africa (28) [Branch 1998; Spawls et al. 2018; Branch et
al. 2019; Bauer et al. 2019].
The taxonomy of the lacertid genus Nucras Gray,
1838 is complicated by the relatively secretive habits
and conservative morphology of known species, and
this has confounded early attempts to resolve species
November 2019 | Volume 13 | Number 2 | e199
Branch et al.
boundaries and geographical distributions within the
genus. Currently, Nucras comprises eleven species that
are mainly restricted to southern Africa, with a northern
outlier (Nucras boulengeri Neumann, 1900) occurring
in East Africa, although there is a single, isolated record
from Isoka, northern Zambia (Haagner et al. 2000;
Spawls et al. 2018).
Taxonomy of the Western (or Striped) Sandveld
Lizard, Nucras tessellata, has proven to be particularly
problematic, as have the species boundaries within the N.
tessellata species complex. Broadley (1972) recognized
four subspecies (Nucras taeniolata taeniolata, Nucras
taeniolata ornata, Nucras tessellata tessellata, and
Nucras tessellata livida), as well as a number of
taxonomically unresolved non-specific forms, Le.,
Nucras tessellata tessellata var. “TV,” Nucras taeniolata
ornata var. holubi, and Nucras tessellata tessellata vat.
elegans. Broadley (1972) examined the morphology of
over 800 specimens and concluded that the dorsal color
pattern and the number of subdigital lamellae under the
4" toe are reliable taxonomic characters to differentiate
species within the N. tessel/lata complex. In recent years,
several subspecies and varieties were elevated to full
species, e.g., Nucras taeniolata, N. holubi, N. ornata
(Jacobsen 1989), and N. /ivida (Branch and Bauer 1995).
A number of historically problematic Angolan specimens
were considered to form part of the Nucras tessellata
(Smith, 1838) complex, best representing Nucras
tessellata tessellata var. “T.” However, Broadley (1972)
deferred making a decision on their taxonomic status
pending the collection of additional material. The only
other Angolan member of the genus, Nucras scalaris
Laurent, 1964, was described on the basis of material
from northern Angola and is not currently regarded to be
included in the N. tessellata complex.
Bocage (1895) was the first to record N. tessellata from
Angola, but noted only that (translated from the original
French): “Mr. Anchieta met this species at two different
locations, Maconjo and Caconda, from where he sent us
a few individuals. All of these individuals belong to the
variety taeniolata, separated from the typical form not
only by its coloration, with a back striped longitudinally
in white and blackish-brown, but is also slimmer.” He
provided no further details of the specimens, leaving out
information on scalation and size. Fortunately, the late
Donald G. Broadley visited the Museu Bocage Lisboa,
Portugal (currently Museu Nacional de Historia Natural
e da Ciéncia) in 1968, before the disastrous fire of 1978
destroyed its collections. Broadley was only able to locate
the three specimens from Maconjo listed by Bocage
(1895). Boulenger (1910) first assigned specimens from
Mocamedes (=Namibe) district to Nucras tessellata var.
taeniolata. In subsequent years, he referred the same
material as part of Nucras intertexta var. holubi under
a different color variation A and called this the most
“primitive form’ (Boulenger 1917, 1921). Monard (1937)
Amphib. Reptile Conserv.
recorded three additional juvenile specimens from
Kapelongo (= Capelongo) and reported that they exhibit
typical coloration of taeniolata, and thus assigned his
material to the N. tesse/lata complex. The most detailed
description to follow was a specimen collected from “km
34 de la route de Mocamedes a Sa da Bandeira” (= 34
km from Namibe on Lubango road) and documented by
Laurent (1964). All the above specimen data are pooled
in the summary tables of scalation in the revision of the
N. tessellata complex (Broadley 1972), and he concluded
that the Angolan material represents an undescribed
species.
During recent surveys in south-western Angola,
several individuals of Nucras were collected. This new
material is compared with historical material of the
species known from Angola and supplemented with
phylogenetic analyses to investigate their taxonomic
status, and to advance our understanding of the N.
tessellata complex.
Materials and Methods
Sampling and material examined. During a recent
expedition to south-western Angola, two Nucras
individuals were collected from Namibe Province (Fig.
1). Each specimen was collected as a voucher, fixed in
10% formalin and thereafter transferred to 70% ethanol
for long-term storage at the Port Elizabeth Museum
(PEM). Prior to fixation, a tissue sample was collected
and preserved in 99% ethanol. Material from the
following museums was examined (Table 1) by Donald
Broadley: Museu Bocage Lisboa, Portugal (MBL),
Museu Regional do Dundo, Dundo, Angola (MD), and
the British Museum (now Natural History Museum,
London) [NHML]. WRB examined material in the
Transvaal Museum (now Ditsong National Museum of
Natural History Northern Flagship Institute, Pretoria)
[TM], and re-examined and photographed the NHML
specimens. Photographs of Monard’s (1937) material
from the Musée d’Histoire Naturelle, La-Chaux-de-
Fond, Switzerland (MHNC, formerly LCFM) were made
available by Luis Ceriaco. The Angolan material was
further compared to other material housed in the PEM.
Morphological data. To quantify morphology for the
Species diagnoses, the following measurements were
recorded from each individual: snout-vent length (SVL):
tip of snout to anterior edge of cloaca; tail length (Tail):
tip of tail to posterior edge of cloaca; total length (TL):
combined SVL and tail length; head length (HL): from
anterior edge of occipital/parietal scale to tip of snout;
head width (HW): width of head (just behind eye); snout
length (SL): from anterior corner of eye to tip of snout;
eye length (EL): horizontal diameter of eye; ear-eye
length: from posterior corner of eye to anterior edge of
ear opening.
November 2019 | Volume 13 | Number 2 | e199
A new Nucras species from Angola
Legend
@ Nucras broadleyi sp. nov.
Altitude
Mi i00m
500 m
| 900m
1300 m
Ml 1700 m
150
Fig.1. Map showing distribution of Nucras broadleyi sp. nov. in Angola.
The following scalation details were recorded:
upperlabials (UL): in front of subocular and after
subocular; lowerlabials (LL), transverse rows of
ventrals, longitudinal ventral scale rows, supraciliars
(SC), granules between supraciliars (SC) and subocular,
number of subdigital lamellae below 4" toe, and number
of femoral pores. All counts were performed on both left
and right sides. The presence of interparietal and whether
it was in contact with occipital were also recorded.
Phylogenetic analyses. To place the two Nucras
individuals recently collected from Angola in a
phylogenetic context, one nuclear (RAG-1) and two
mitochondrial (ND4, 16S) genes were sequenced (Table
2). DNA was extracted using salt extraction (Aljanabi
and Martinez 1997), with PCR amplification, and cycle
sequencing following standard procedures. A 25 ul PCR
reaction included 3 ul of 1 mM dNTPs, 3 ul of 25 mM
MgCl, 0.2 ul of 10 pmol forward and reverse primers,
3 ul of buffer solution (20 mM Tris-HCI ~pH 8.0, 100
mM NaCl, 0.1 mM EDTA, 1 mM DTT), 0.1ul (0.5U)
Taq polymerase, and 1—2 ul of 25 ng/ul genomic DNA.
Thermal cycling was run with initial denaturation for 4
min at 94 °C followed by: 35 cycles with denaturation for
30 s at 94 °C, annealing for 40 s at 55—57 °C, extension
Amphib. Reptile Conserv.
for 40 s at 72 °C, and final extension for 4 min at 72 °C.
Primers used for amplification were ND4: ND4 (Forstner
et al. 1995) and Leul (Arévalo et al. 1994), 16S: L2510
and H3080 (Palumbi 1996); and RAG-1: RAGI-FO and
RAGI-R1 (Mayer and Pavlicev 2007). PCR products
were run on a 1% agarose gel and visualized under a UV
light to verify amplification. Amplicons were sequenced
directly using the forward primers at Macrogen
(Amsterdam, Netherlands). Sequences were edited and
aligned using Geneious software v4.7 (Kearse et al.
2012). New sequences have been deposited in GenBank
(Table 2). In addition, gene sequences for multiple
individuals of all Nucras species (except N. scalaris) and
sequences representing outgroup taxa were downloaded
from GenBank (Table 2).
A Bayesian analysis of 2,052 characters from the two
mitochondrial genes and one nuclear gene (ND4: 678
bp, 16S: 482 bp, RAG-1: 892 bp) was used to investigate
optimal tree space using MrBayes v3.2.2 (Huelsenbeck
and Ronquist 2001) at the CIPRES Science Gateway
(Miller et al. 2010). To determine which evolutionary
model best fit the data, j;Modeltest was initially run (Posada
2008). The AIC test specified the GIR+G model for both
mitochondrial markers and HYK+G for RAG-1. Therefore,
three unlinked data partitions were created, specifying six
November 2019 | Volume 13 | Number 2 | e199
Branch et al.
100
1.0
97
1.0
94
6.97
61
0.98
92
1.0
100
1.0
100
1.0
L, longicaudata
0.04 substitutions/site
N. intertexta MCZ38872
as N intertexta MB20952
N. intertexta PEM R18661
100 N. intertexta MB21183
1.0 N. intertexta PEM R18257
N. ornata NMB R10658
100|I NV. ornata NMB R10907
101 NV omata AMB8635
N. holubi MCZ38793
N. holubi PEM R18647
N. holubi PEM R22814
‘ N. taeniolata PEM R18080
To | NV. taeniolata 2251
N. taeniolata HZ250
N. taeniolata HZ252
N. tessellata AMB5584
N tessellata PEM R16873
N. tessellata PEM R16872
N tessellata PEM R18745
N tessellata NMB R11574
N livida PEM R18747
100 aa
7) N. lvida. MBUR00687
N livida MB21176
N. livida, MB21225
N lida PEM R22822
roy N. lalandii 48037
1.0 N. lalandii, PEM R22815
100 N lalandii. MBUR00483
1.0 N lalandii HZ246
100 N lalandii HB124
1.0 N. lalandii MB20982
100 -— N. broadleyi sp. nov. PEM R24157
Ise N. broadleyi sp. nov. PEM R24005
N. boulengeri_ 1102169
81
100 70
1.0
A. australis MH0531
A. australis GWO08
100 I capensis CAS 209602
I capensis AMB6001/NMNW
M. suborbitalis PEM R18376
Fig. 2. Maximum likelihood topology for Nucras with bootstrap values (top) and Bayesian posterior probabilities (bottom) at each
node. Bootstrap values <60%, posterior probabilities <O.90, and node support within each species is not shown.
(mitochondrial genes) and two (RAG-1) rate categories,
including the gamma distribution, with uniform priors for
all parameters. For 16S, 38 bases were excluded due to
poor alignment. To ensure the robustness of results, the
MCMC was run twice in parallel for 20 million generations
(four chains in each run), with trees sampled every 1,000
generations. A 10% burn-in was examined (2 million
generations, 2,000 trees) in Tracer v1.6 (http://beast.bio.
ed.ac.uk) to check that the effective sample size (ESS) of
all parameters met a threshold of 200 after burn-in. A 50%
majority rule tree was constructed and nodes with > 0.95
posterior probability were considered supported.
In addition to the Bayesian analysis, a maximum
likelihood (ML) search was run using RAxML HPC 7.2.8
(Stamatakis 2006) on the CIPRES Science Gateway (http://
www.phylo.org/sub_sections/portal/) for the combined
dataset. The datasets were partitioned as in the Bayesian
analysis, with a GTR+I+G model for all markers and 1,000
bootstrap replicates (Stamatakis et al. 2008). This analysis
was run three times to ensure that independent ML searches
produced the same topologies. Nodes with a bootstrap value
Amphib. Reptile Conserv.
of > 70% were considered as supported in this analysis.
Pairwise sequence divergence values (uncorrected
net p-distances) were estimated between species for both
markers using MEGA v7 (Kumar et al. 2016). In addition,
a barcoding approach was used to compare inter- and intra-
specific sequence divergences, using SpeciesIdentifier v1.8
(Meier et al. 2006). Pairwise comparisons were generated
for all Nucras individuals in the phylogeny for each gene,
and frequency distributions of inter- and intra-specific
comparisons were made. The ND4 gene was truncated
433 bp, as some GenBank sequences had only partial
sequences for that gene.
Results
Phylogenetic analyses. The phylogenetic analyses show
that the two individuals from Angola are in the same clade,
and it is sister to a clade containing WN. livida, N. taeniolata,
and N. tessellata (Fig. 2). The new Angolan clade is well-
supported by both Bayesian and likelihood analyses.
Uncorrected net p-distances for each of the genes are
85 November 2019 | Volume 13 | Number 2 | e199
A new Nucras species from Angola
0 lott tamaddn aul
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c)
Pairwise distance
Fig. 3. Frequency distribution of pairwise sequence divergences
for Nucras species for a) 16S, b) ND4, and c) RAG-1. Inter-
specific differences shown as black bars, and intra-specific
differences as white bars. The ranges of values relating Nucras
broadleyi sp. nov. with other members of the N. tesse/lata clade
are indicated by brackets.
similar to those found for other species of Nucras (Table
3), and the frequency distribution of pairwise differences
shows that these Angolan individuals fall in the range of
inter-specific divergence values (Fig. 3).
Systematics. Based on the minor morphological
differences and the distinct dorsal coloration differences
observed among material examined, combined with the
abovementioned genetic evidence, the Angolan material
is described below as a new species. No historical names
are available for this clade, thus leaving no outstanding
taxonomic issues (Broadley 1972; Uetz et al. 2017).
Nucras broadleyi sp. nov.
Angolan Sandveld Lizard
urn:lsid:zoobank.org:act: C82E3A75-96FF-4D2A-9B52-3A BF4B58BC2B
Amphib. Reptile Conserv.
(Figures 4-6)
Chersonymy. Nucras tessellata var. taeniolata (Bocage
1895: 30), Nucras tessellata var. taeniolata (Boulenger
1910: 474), Nucras tessellata var. holubi (Boulenger 1917:
210), Nucras intertexta var. holubi (Boulenger 1920: 20),
Nucras tessellata (Monard 1937: 73; Laurent 1964: 56),
Nucras ornata (Broadley 1965: 23), Nucras tessellata
(Broadley 1972: 30; Ceriaco et al. 2016: 56; Burger 2014:
171), Nucras aff. tessellata (Marques et al. 2018: 221;
Branch et al. 2019: 317).
Type material. The type series is comprised of the three
most recently collected specimens, which are housed in
PEM and TM.
Holotype. A subadult male (PEM R24005, AG 018), 10
km west of Lola, edge of Bentiaba River valley, Namibe
Province, Angola (-14.29028, 13.53056, WGS 84, 802 m
asl). Collected by W.R. Branch, P. Vaz Pinto, and J.S. de
Almeida on 2 November 2015.
Paratypes (2). a) A subadult female (PEM R24157,
AG 166), 8.8 km southwest of Farm Mucungo, Namibe
Province, Angola (-14.80167, 12.41917, WGS 84, 385 m
asl). Collected by W.R. Branch, P. Vaz Pinto, and J.S. de
Almeida on 8 November 2015. b) An unsexed adult (TM
40392), “34 km S of Mocamedes to Porto Alexandre,
Angola, 1512Ca” (= 34 km S Namibe to Témbwa),
Namibe Province, Angola (approx. -15.48220, 12.18289).
Collected by W.D. Haacke on 30 March 1971.
Additional referred material: The following additional
material was used to expand the description of variation
within the species: a) an adult male (MD 1967, Laurent
1964), “km 34 de la route de Mocamedes a Sa da Bandeira”
(=34 km from Namibe on Lubango road, -15.03333,
12.41667), collected 24 October 1949, b) MBL 646,
647a, 647b (Bocage 1895: 30) from Maconjo (approx.
-15.01667, 13.20000), c) BM 1970.6.29.10—11 (Boulenger
1910: 474) from Ponang Kuma (= Donguena, approx.
-17.01667, 14.71667), and d) MHNC 91.0524 (Monard
1937) from Capelongo (approx. -14.88333, 15.083333),
collected April 1933.
Etymology. The specific epithet is a patronym tn honor of
Donald G. Broadley for his numerous contributions to the
herpetofauna of Africa. Don (as most of us knew him) was
the first to recognize the Angolan population as a separate
species (Broadley 1972). The name is constructed in the
masculine genitive.
Diagnosis. Assigned to Nucras due to a well-defined collar
(absent in /chnotropis), toes not serrated or fringed (versus
serrated or fringed in Meroles), subdigital lamellae smooth
(versus keeled in Pedioplanis and Heliobolus), subocular
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Branch et al.
Li
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supraciliaries and supraoculars (versus mostly absent in N.
bordering lip, the nostril is pierced between two nasals,
nasal well separated from upper labial, and dorsal scales
small,
boulengeri and N. lalandii), 23-29 lamellae under 4" toe
dorsum with a series of
longitudinal pale stripes (versus dark cross bands present
5)
(versus less than 22 in N. lalandii)
smooth, and juxtaposed.
The new species can be diagnosed from other Nucras
species based on a combination of the following characters:
in N. lalandii and N. scalaris or a series of pale vertebral
spots, sometimes forming irregular transverse bands in N.
intertexta or lack of any dorsal patterns in N. aurantiaca),
series of transversely enlarged plates present under forearm
(versus absent or only feebly enlarged in Nucras lalandii),
four pale stripes on nape with outer stripes forming a
a small series (0-6) of small granules present between
November 2019 | Volume 13 | Number 2 | e199
87
Amphib. Reptile Conserv.
A new Nucras species from Angola
SoUIAOLg ade_ wayseq ‘voy yNog | 9szSOODH | IE€ZSOODH | O1ZSOO0DH Os0sTa Wad] osostuWad} ewotuany | Sdn
SOUIAOI OdeD Woyseq “BLY YINOS | PSZTSOODH | OEZSOODH | 807S00DH IScZH DIDjOWev] SDAINN
BOLFV YINOS | EScTSOODH LOCSOODH OSCZH
SOUTAOI [BIEN-NINZEMY “BOLIFY YINOS IScSO0DH vOCSOO0ODH 85901 GAIN oeclOdNadN
SOUTAOI_ [RVN-NINZEMY “BILFV YINOS | OSTSOODH €0cSOODH LO6OTYH AIAN 9cclONNAN DIDUAO SDAONN
soutaoig adeg wioyseq ‘eorpy yinog | 6EstsedH | PESIsSedH |] sssisodH 9P@ZH upupjoy | = SAO
soutaoig ode usaiseq ‘vorpy ynog | _LesTs6dH | ZestsedH | €SSIS6cH p7lGH upupjoy | = SAO |
SoUIAOI [EIVN-NINZeMy ‘voy ynog | gestsedH | CEsIsodH| pSSISodH LEOdH upupjoy| = SAO |
SOULAOIg ade WOYHON “woLyy yINOS | 6EZSOODH | 8IZSOODH | 061S00DH LLTASU pixauiamt | SBAON |
OUIAOIg ade WOYHON “woLyy yINOS | OPZSOODH | 6IZSOODH | 161S00DH O€0dSu pixauiamt | SAN |
soulAoig ododury ‘eauyy nos | 1PZSOODH | OZZSOODH| Z61S00DH ZL88EZOW pixaiiamt | SAO |
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soutaorg ododuiry ‘eouyy yinog | sEzsoQODH | FIZSOODH} 981S00DH 8E1PET SVO €6L8EZOW iqnjoy| = Sao
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sduIAGIg oqrUeN “ejosuy | KEZgs9TNIN | AILSS9TNIN | AOLSS9TNIN LSIp7u Wad 991DV ‘ou ‘ds Majppodg | SDLONN |
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SDAINN
November 2019 | Volume 13 | Number 2 | e199
1998 Ta Wadd
LSc8 lad Wad
CICVET SVO
Lv98 lad Wad
88
Amphib. Reptile Conserv.
Branch et al.
continuous light stripe with the outer edges of the parietals
(similar to Broadley’s (1972) N. tessellata tessellata var.
“T-” differs from N. livida and N. tessellata where the outer
stripes often do not form a continuous light stripe with the
outer edges of the parietals; differs from N. caeiscaudata
and N. ornata where there are only three longitudinal
stripes present on nape and sometimes the vertebral ones
are absent), well defined occipital scale separating parietals
(versus reduced or absent in northern Namibia N. holubi,
which is referred to as N. intertexta damarana Parker; as
well as absent in NV. caesicaudata), parietal foramen absent
(often present in all other species except N. taeniolata),
and postnasals separated (usually fused in NV. taeniolata).
In the phylogenetic analysis, the uncorrected p-distances
show that this clade differs by >8% for 16S, >14% for
ND4, and >1% for RAGI sequence divergence from other
members of the N. tesse/lata clade.
South Africa, Northern Cape Province
South Africa, Western Cape Province
South Africa, Northern Cape Province
South Africa, Northern Cape Province
South Africa, Northern Cape Province
South Africa, Western Cape Province
South Africa, Western Cape Province
South Africa, KwaZulu-Natal Province
South Africa, Western Cape Province
Namibia, Kamanjab
Description of Holotype (Fig. 4). Body relatively slender
(SVL approx. 4.5 times the head length, tail truncated),
with hindlimbs larger than forelimbs (femur of hind limb
equal to length of tibia); head narrow and elongated (56%
longer than wide) with narrow pointed but blunt snout, that
is slightly longer than distance from back of eye to rear of
ear opening. Rostrum protruding and visible from below.
Nasals paired and in contact (0.2 mm suture length), not
swollen, nostril directed backwards separating postnasals.
Frontonasal single, wider than long (1.1 x 1.8 mm).
Prefrontals paired and in broad median contact with one
another (0.6 mm suture length), wider than long (1.1 x 1.2
mm). Frontal entire, longer than wide (2.7 x 1.9mm). Two
large rounded supraoculars, both in contact with the frontal,
with anterior supraocular preceded by a single large scale
in contact with prefrontal, frontonasal, and posterior loreal,
with posterior supraocular bordered by a single large
scale in contact with parietal and frontoparietal. Paired
frontoparietal in broad contact (1.3 mm suture length),
nearly as wide as long (1.7 x 1.5 mm). Parietals twice as
long as wide (3.1 x 1.8 mm), fully separate by a large,
pentagonal interparietal (2.5 x 1.2 mm) that is twice as long
as wide, slightly shorter than frontoparietals and nearly
equal to length of frontonasal and prefrontal combined.
Small subtriangular occipital (0.5 x 0.7 mm). Two loreals,
second much larger than first. Six supraciliaries on each
side, 1‘ is the longest. A single minute granule scale
between supraocular and supracilliares on right side, none
on left side. Four supralabials anterior to subocular and
three supralabials posterior to subocular, on both sides.
Subocular slightly elevated medial and bordering the
lip, its lower border being shorter than the upper. Three
temporal scales, first longer than others, smooth. Tympanic
shield as wide as long, border of ear opening. No ear lobes.
Lower eyelid with transparent brille formed by five larger
scales, surrounded by numerous smaller scales. Lower
eyelid separated from subocular and enlarged temporal
scales by a series of 10 smaller scales. Small scale above
3 supralabial separating the posterior loreal and subocular.
a
accession number
Museum
Field accession
|Ichnotropis. ‘| capensis. ~—S—Ss«| AMBB6067 CAS 209602 DQ871149 | HF5S47733__ | DQ871207
| Meroles —*| suborbitalis. ‘| SVNO049 PEM R18376 HF547800 | HF547759 _| HF547718
Australolacerta
Table 2 (continued). Samples used in genetic analysis. Museum abbreviations: CAS — California Academy of Science, PEM — Port Elizabeth Museum, NMB — National Museum Bloemfontein.
Australolacerta
2.
=)
)
Lae!
oa
=
O
Amphib. Reptile Conserv. 89 November 2019 | Volume 13 | Number 2 | e199
A new Nucras species from Angola
Table 3. Pairwise uncorrected net p-distances for species of Nucras: a) 16S, b) ND4, c) RAG-1. Comparisons not made due to
missing data indicated by na.
a) 1 2 3
1 broadleyi sp. nov 0.048
2 lalandii 0.083 0.047
3 livida 0.097 0.058 0.019
4 taeniolata 0.098 0.056 0.084
5 tessellata 0.075 0.043 0.026
6 boulengeri 0.105 0.101 0.117
7 holubi 0.074 0.044 0.066
8 intertexta 0.084 0.068 0.090
9 ornata 0.083 0.067 0.091
b)
1 broadleyi sp. nov na
2 lalandii 0.139 0.124
3 livida 0.194 0.115 0.045
4 taeniolata 0.208 0.147 0.121
5 tessellata 0.198 0.138 0.112
6 boulengeri 0.219 0.188 0.233
7 holubi 0.153 0.092 0.137
8 intertexta 0.208 0.141 0.175
C)
1 broadleyi sp. nov 0.001
2 lalandii 0.012 0.002
3 livida 0.014 0.009 0.004
4 taeniolata 0.013 0.007 0.009
5 tessellata 0.012 0.006 0.008
6 boulengeri 0.066 0.059 0.064
7 holubi 0.020 0.015 0.017
8 intertexta 0.017 0.012 0.013
9 ornata 0.021 0.016 0.016
4 5 6 7 8 9
0.000
0.073 0.027
0.116 0.103 na
0.063 0.053 0.079 0.048
0.085 0.078 0.105 0.043 0.008
0.082 0.076 0.108 0.050 0.043 0.000
0.003
0.006 0.018
0.277 0.267 na
0.156 0.146 0.199 0.115
0.196 0.193 0.239 0.118 0.017
0.004
0.007 0.008
0.064 0.058 na
0.016 0.016 0.068 0.004
0.012 0.013 0.064 0.015 0.001
0.016 0.017 0.064 0.019 0.004 0.001
Enlarged scale bordering 1“ post subocular, supralabial,
and the subocular. Six infralabials on both sides, with
3" being longest; four enlarged pairs of chin shields,
last largest and first three in broad contact. Twenty-four
gular scales in a straight line between symphysis of chin
shields and median collar plate, equal in size except last
4—5 larger. Collar free, comprising seven enlarged plates
(median subtriangular) and extending slightly onto side of
neck as a crease, bordered by 2—3 smaller scales. Dorsal
scales small, juxtaposed, granular, smooth, larger on sides
toward ventrals. Midbody scales 42. Ventral plates eight
longitudinal and 28 transverse rows (from collar to groin),
plates of the innermost rows longer than broad, with outer
row notably smaller than other rows, transverse row of
ventrals across chest just behind collar longer than broad:
preanal scales irregular, median ones larger. Scales on
upper surface of forearm large, smooth or slightly keeled.
Scales on lower surface of forearm with eight enlarged
plates, at least twice the width of scales on upper forearm.
Amphib. Reptile Conserv.
Scales on upper surface of tibia rhombic, subimbricate,
smooth, and much larger than dorsal scales. Tibia below
with a series of large plates. Subdigital lamellae under
fourth toe 23R/25L. Femoral pores 13R/15L. Dorsal scales
on tail oblique, strongly keeled diagonally, and truncate
behind, ventral scales on tail obtusely keeled.
Coloration. Dorsum with eight pale cream to white
dorsolateral longitudinal stripes, separated by dark brown
to black stripes. These stripes are more boldly patterned
anteriorly, fading posteriorly. No light vertebral stripe.
The two pale paravertebral stripes are separated by a very
narrow strip of darker scales that starts on the interparietal
through the occipital scale and fades posteriorly onto body
and tail. The dorsolateral stripe extending along outer
borders of parietals continues onto the tail. It is followed
by the upper lateral stripe extending from posterior of the
eye onto the head through the mid-temporal with a brief
break above the ear opening, and continues onto the tail.
The lower lateral stripe starts at the subocular, through the
November 2019 | Volume 13 | Number 2 | e199
Branch et al.
nak acl; Var red: bee M7 pet
Fig. 4. Nucras broadleyi sp. nov. A—
holotype, adult male, PEM R24005 (AG 18) in life; B— general habitat photo of type locality,
tre
-y" =
tetet tht beter fa!
10 km west of Lola, edge of Bentiaba River valley, Namibe Province, Angola; C — lateral close-up of head of holotype; D — dorsal
close-up of head of holotype; E — ventral close-up of head of holotype (Photos: Bill Branch).
ear opening, broken briefly above the arm, after which
it continues all the way onto the tail. Ventrum white and
lower limbs oblique white. Fore limbs upper surface black
with scattered pale blotches. Hind limbs light brown with
pale blotches. Upper surface of tail red-brown, similar to
hind limbs. Scales bordering the orbit are black edged.
Variation (Figs. 5-6). Meristic and escalation data are
summarized in Table 1. The largest specimen examined
is (BM 1907.6.29.10) 74 +144 mm (tail regenerated).
Regarding coloration, there seem to be three main variations
among material examined: 1) 8—9 longitudinal stripes as
in holotype (in PEM R24005, MBL 647a, 647b, MHNC
91.0524—5), 2) 4-5 pale longitudinal stripes broken up
posteriorly with flanks spotted (in BM 1970.6.29.10-11,
TM 40392, MD 1967), and 3) broken paravertebral stripes,
continuous dorsolateral line and barred flanks (in PEM
R24157), similar to N. intertexta.
Distribution. Found only in semi-arid south-western
Angola, throughout much of Namibe Province and
extending onto the escarpment of southern Huila and
Cunene Provinces (Fig. 1). Known localities include:
Maconjo (Bocage 1895: 30), Ponang Kuma (=Donguena)
Amphib. Reptile Conserv.
91
(Boulenger 1910: 472), 34 km from Namibe on Lubango
road (Laurent 1964: 56), 34 km south of Tombwa (TM
40397), 8.8 km southwest of Farm Mucungo (this study),
10 km west of Lola (this study), and Capelongo (Monard
1937: 73). The locality of Caconda (Bocage 1895) extends
the species distribution further north into Huila Province,
but the specimens could not be critically evaluated by
Broadley (1972) and are now presumably lost.
Habitat. The species appears to be associated with
mopane woodlands, dry savannas, and semi-desert
shrublands (Barbosa 1970). The new material was found
in sandy plains with scattered low granite outcrops, with
varying degrees of short grass cover and scattered bushes.
Vegetation included Colophospermum mopane, Ficus sp.,
Senegalia (=Acacia) mellifera, Commiphora sp., Boscia
foetida, and Salvadora persica. The confirmed historical
records were also obtained within the dry woodland zone,
even though the possible occurrence of the species in
Caconda would place the species above 1,500 m asl and
well into the mesic conditions of Brachystegia habitats
(Barbosa 1970).
Conservation. Population estimates for the species
November 2019 | Volume 13 | Number 2 | e199
A new Nucras species from Angola
- th TWh olt hei ‘even
Fe a
iui
Fig. 5. Nucras broadleyi sp. nov. A — paratype, adult female, PEM R24157 (AG 166) dorsal view; B — ventral view; C — dorsal
close-up of head of paratype; D — ventral close-up of head of paratype; E — lateral close-up of head of paratype; F — general habitat
photo of type locality, 8.8 km southwest of Farm Mucongo, Namibe Province, Angola (Photos: Bill Branch).
are unknown, and only few scattered specimens (~12)
are known, of which four specimens were destroyed in
the Museu Bocage Lisboa fire and one of the Monard
Specimens is unaccounted for. However, Sandveld Lizards
are secretive and less conspicuous than many other
lacertids, so additional surveys are required to determine
the full range of the species and to identify potential habitat
threats in order to accurately assess its conservation status.
Discussion
Broadley (1972) was the first to suggest the Angolan pop-
ulation of Nucras tessellata to be different from other de-
scribed species, but took no taxonomic action. Here, we
present evidence to support his assumptions and formally
describe the Angolan population as a new species. Thus,
Angola now has two endemic species of Nucras and the
genus now comprises 12 recognized species. As our phy-
logeny is built on the work of Edwards et al. (2013) we
retrieved the same general topology, except for the inclu-
sion of the new species. Although different samples and
genetic markers were used, Bauer et al. (2019) retrieved
the same species relationships except for the inclusion
of their newly described species, N. aurantiaca. Thus,
we can conclude that the current species relationships are
Amphib. Reptile Conserv.
92
well resolved. Due to the secretive nature of members
of this genus, disjunct distribution, and previously rec-
ognized varieties (see Broadley 1972), it is possible that
there are other undiscovered species, particularly in areas
that remain poorly surveyed.
The species appears restricted to the arid biomes of
southwestern Angola at relatively low to moderate alti-
tudes, while the records from Caconda remain problematic
and may have been misidentified or incorrectly labelled.
In recent years, the number of endemic species described
from the arid south-western Angola has increased, e.g.,
Kolekanus plumicaudus (Haacke 2008), Pedioplanis
huntleyi and P. haackei (Conradie et al. 2012), Cordy-
lus namakuiyus (Stanley et al. 2016), Cordylus phono-
lithos (Marques et al. 2019b), Poyntophrynus pachnodes
(Ceriaco et al. 2018), and now Nucras broadleyi sp.
nov. This region also harbors numerous other endemic
species, such as Afrogecko ansorgii, Pachydactylus an-
golensis, Poyntonophrynus grandisonae, Pedioplanis
benguellensis, Rhoptropus taeniostictus, Typhlacontias
rudebecki, and T. punctatissimus bogerti (Ceriaco et al.
2016, 2018; Marques et al. 2018; Branch et al. 2019).
The growing body of information suggests there could
be a unique and diverse endemic Angolan-Namib reptile
fauna (Ceriaco et al. 2016; Marques et al. 2018; Branch
November 2019 | Volume 13 | Number 2 | e199
Branch et al.
Fig. 6. Variation of Nucras broadleyi nov. sp. dorsal color pattern. A—TM 40392 from “34 km S of Moc¢amedes to Porto Alexandre;”
B — BM 1970.6.29.10 from Ponang Kuma (=Donquena); C - MHNC 91.0524 from Capelongo; D— MD 1967 from “km 34 de la
route de Mocamedes a Sa da Bandeira” (Photos: A,B — Bill Branch, C, D — Luis Ceriaco).
et al. 2019), with additional discoveries yet to be made.
Acknowledgements.—We thank José Luis Alexandre
and Fernanda Lages for organizing the export permits
for the vouchers, done within the framework of a
SASSCAL Project sponsored by the Federal Ministry
of Education and Research (BMBF) - ISCED permit
issued 12 November 2015. We thank Lemmy Mashinini
(Ditsong Museum, Pretoria, South Africa) and Patrick
Campbell (Natural History Museum, London, United
Kingdom) for allowing WRB to inspect material in their
care. Shiela Broadley kindly provided access to the late
Don Broadley’s data, noting that Don was one of the last
researchers that managed to study the Bocage material
before a fire destroyed the collection. Aaron Bauer and
Luis Ceriaco are thanked for providing additional data
and comparative photographs of Angolan material, and
their excellent reviews which improved the quality of
this paper. Jodo Simdes de Almeida is thanked for his
field assistance. This work was supported in part by the
National Research Foundation of South Africa and the
South African National Biodiversity Institute.
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Bill Branch (William R. Branch) was born in London, United Kingdom. Bill was
employed as Curator of Herpetology at the Port Elizabeth Museum for over 30 years
(1979-2011), and upon his retirement he was appointed Curator Emeritus Herpetology
until his death in October 2018. Bill’s herpetological studies concentrated mainly
on the systematics, phylogenetic relationships, and conservation of African reptiles,
but he has been involved in numerous other studies on the reproduction and diet of
African snakes. He has published over 300 scientific articles, as well as numerous
popular articles and books. The latter include: South African Red Data Book of
Reptiles and Amphibians (1988), Dangerous Snakes of Africa (1995, with Steve
Spawls), Field Guide to the Reptiles of Southern Africa (1998), Tortoises, Terrapins,
and Turtles of Africa (2008), and Atlas and Red Data Book of the Reptiles of South Africa, Lesotho, and Swaziland (multi-authored,
2014), as well as smaller photographic guides. In 2004, Bill was the 4" recipient of the “Exceptional Contribution to Herpetology”
award of the Herpetological Association of Africa. Bill has undertaken field work in over 16 African countries, and described nearly
50 species, including geckos, lacertids, chameleons, cordylids, tortoises, adders, and frogs.
Amphib. Reptile Conserv.
Werner Conradie holds a Masters in Environmental Science (M. Env. Sc.) and has 12 years of
experience with the southern African herpetofauna, with his main research interests focusing on the
taxonomy, conservation, and ecology of amphibians and reptiles. Werner has published numerous
principal and collaborative scientific papers, and has served on a number of conservation and
scientific panels, including the Southern African Reptile and Amphibian Relisting Committees.
He has undertaken research expeditions to many African countries including Angola, Botswana,
Lesotho, Malawi, Mozambique, Namibia, South Africa, Zambia, and Zimbabwe. Werner is currently
the Curator of Herpetology at the Port Elizabeth Museum (Bayworld), South Africa.
Pedro Vaz Pinto is Angolan and was born in Luanda, Angola, in 1967. Pedro graduated in Forest
Engineering at the Technical University of Lisbon, and obtained a doctoral degree in Biology from
the University of Porto, Portugal. Over the past 20 years, he has worked in biodiversity conservation
in Angola addressing rare or endangered species, and protected area management. Pedro is a director
for the local NGO Kissama Foundation, and a researcher for CIBIO-InBio. His studies on Angolan
vertebrates have focused mostly on genetics, biogeography, and conservation in antelopes, birds,
reptiles, and amphibians. Pedro travels the country extensively and has received three international
environmental awards for his biodiversity conservation work in Angola.
Krystal Tolley is a Principal Researcher at the South African Biodiversity Institute in South Africa.
Krystal studies patterns of biodiversity and adaptation of African reptiles by combining phylogenetics,
phylogeography, performance-based data, species distribution models, and morphology.
November 2019 | Volume 13 | Number 2 | e199
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 96-130 (e203).
The herpetofauna of Bicuar National Park and surroundings,
southwestern Angola: a preliminary checklist
12.3*Ninda L. Baptista, '¢Telmo Antonio, and °°tWilliam R. Branch
‘Instituto Superior de Ciéncias da Educagao da Huila (ISCED-Huila), Rua Sarmento Rodrigues, Lubango, ANGOLA *CIBIO/InBio — Centro de
Investigagdo em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairdo, 4485-661 Vairdo, PORTUGAL *Faculdade
de Ciéncias, Universidade do Porto, 4169-007 Porto, PORTUGAL ‘Faculty of Natural Resources and Spatial Sciences, Namibia University of
Science and Technology, Private Bag 13388, Windhoek, NAMIBIA *Port Elizabeth Museum (Bayworld), P.O. Box 13147, Humewood 6013, SOUTH
AFRICA ‘Research Associate, Department of Zoology, P.O. Box 77000, Nelson Mandela Metropolitan University, Port Elizabeth 6031, SOUTH
AFRICA * Deceased
Abstract.—Bicuar National Park (BNP) is a protected area in southwestern Angola where biodiversity has
been poorly studied. BNP is located on the Angolan plateau on Kalahari sands, in a transition zone between
the Angolan Miombo Woodland and the Zambezian Baikiaea Woodland ecoregions. Herpetological surveys
were conducted in BNP and surrounding areas, through visual encounter surveys, trapping, and opportunistic
collecting of specimens from 2015 to 2018. The regional herpetofauna is described here based on these
surveys, literature records, and additional unpublished records. In total, 16 amphibian, 15 lizard, 18 snake,
two testudine, and one crocodilian species were observed from the recent surveys, and in combination with
historical records the species counts are 21, 36, 32, four, and one species for these herpetofauna groups,
respectively. Important observations include the first record of Xenocalamus bicolor bicolor (Gunther, 1868),
the second records of Sclerophrys poweri (Hewitt, 1935) and of Amblyodipsas ventrimaculata (Roux, 1907),
and the fourth record of Monopeltis infuscata (Broadley, 1997) for Angola. Additionally, the type locality of
Hyperolius benguellensis (Bocage, 1893) is discussed. A part of the material could not be confidently identified
to species level, reflecting the taxonomic uncertainty associated with the Angolan herpetofauna. Fossorial
herpetofauna was well represented, reflecting adaptation to sandy soils, the dominant substrate in the area.
The likely presence of endemic and poorly known species in BNP reinforces the importance of the park for the
conservation of Angolan biodiversity. Further surveys are necessary for a more comprehensive understanding
of the park’s fauna and biogeographic affinities, and to improve conservation planning.
Keywords. Amphibians, reptiles, fossorial, biodiversity surveys, protected areas, Kalahari sands, Huila Province
Resumo.—O Parque Nacional do Bicuar (BNP) é uma area protegida no sudoeste de Angola cuja biodiversidade
se encontra pouco estudada. Localiza-se no planalto de Angola em areias do Calaari, numa zona de transigao
entre as ecorregides de Mata de Miombo Angolana e Mata de Baikiaea Zambeziana. Neste trabalho foram
realizados levantamentos de herpetofauna no BNP e arredores, através de levantamentos de encontro visual,
armadilhagem e recolha oportunistica de espécimes entre 2015 e 2018. Aqui é€ apresentada uma descricgao
da herpetofauna da regiao baseada nestes levantamentos, em registos bibliograficos, e outros registos nao
publicados. Os dados recentes resultaram num total de 16 espécies de anfibios, 15 espécies de lagartos, 18
especies de cobras, duas espécies de quelonios, e uma espécie de crocodilo. A combinagao destes dados
com registos historicos resulta num total de 21, 36, 32, quatro, e uma espécies destes grupos herpetoldgicos,
respectivamente. Entre os resultados mais importantes estao o primeiro registo de Xenocalamus bicolor bicolor
Gunther, 1868, o segundo registo de Sclerophrys poweri (Hewitt, 1935) e de Amblyodipsas ventrimaculata
(Roux, 1907), e o quarto registo de Monopeltis infuscata Broadley, 1997 para Angola. A localidade-tipo de
Hyperolius benguellensis (Bocage, 1893) € tambem discutida. Uma parte do material nao pdde ser identificado
com certeza ao nivel da espécie, uma consequéncia da incerteza taxonomica associada a herpetologia
angolana. A herpetofauna fossorial esta bem representada, reflectindo uma adaptacgao a solos arenosos, o
substrato dominante na area. A presenga provavel de espécies endemicas e pouco conhecidas no BNP reforca
a importancia do parque para a conservagcao da biodiversidade de Angola. Mais levantamentos contribuirao
para um melhor conhecimento da fauna do parque e das suas afinidades biogeograficas e para um melhor
planeamento de estrategias de conservagao.
Palavras-chave. Anfibios, répteis, fossorial, levantamentos de biodiversidade, areas protegidas, areias do Calaari,
provincia da Huila
Correspondence. * nindabaptista@gmail.com
Amphib. Reptile Conserv. 96 December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Citation: Baptista NL, Antonio T, Branch WR. 2019. The herpetofauna of Bicuar National Park and surroundings, southwestern Angola: a preliminary
checklist. Amphibian & Reptile Conservation 13(2) [Special Section]: 96—130 (e203).
Copyright: © 2019 Baptista et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 18 August 2018; Accepted: 11 November 2019; Published: 3 December 2019
Introduction
Angola’s biodiversity is poorly understood, especially
when compared to other countries in southern Africa
(Huntley et al. 2019b). A recent synthesis of the country’s
biodiversity (Huntley et al. 2019b) provides updated
checklists for several taxonomic groups, including
amphibians (Baptista et al. 2019) and reptiles (Branch
et al. 2019c), as does the historical atlas by Marques et
al. (2018), but all these lists highlight the understudied
status of the herpetofauna in Angola. Southwestern
Angola is one of the better-studied regions for vertebrates
in the country (Crawford-Cabral and Mesquitela 1989),
and this is reflected in herpetofauna, from which several
type descriptions originated. Despite many historical
herpetological surveys in the area (Bocage 1895; Schmidt
1933, 1936; Monard 1937a,b; Mertens 1938; Bogert
1940; Laurent 1964; Gans 1976; Poynton and Haacke
1993), contemporary studies continue to yield important
discoveries of new species (Haacke 2008; Conradie
et al. 2012, 2013; Stanley et al. 2016; Ceriaco et al.
2018b; Branch et al. 2019b), new species records for the
country (Huntley 2009; Ceriaco et al. 2016; Branch et al.,
unpub. data), and rediscoveries of species not observed
for several decades (Baptista et al. 2018; Branch et al.
2019a; Vaz Pinto et al. 2019).
The herpetofauna remains undersampled — or
unsurveyed in vast areas of southwestern Angola,
including Bicuar National Park (BNP). Wulf Haacke
conducted two significant herpetological surveys in
this region in 1971 and 1974, collecting over 2,000
specimens (Branch et al. 2019c). Although BNP was not
specifically sampled by Haacke, similar habitats near the
park were included in the surveys. Poynton and Haacke
(1993) described the amphibian collection resulting
from these surveys, but information on the new and rare
reptiles deposited in the Ditsong National Museum of
Natural History (former Transvaal Museum) was never
formally published (Branch et al. 2019c). The Angolan
civil war prevented research in the country for 35 years
(1974-2009) between Haacke's expeditions and the first
post-war biodiversity surveys in southwestern Angola
(Huntley 2009). The first herpetological surveys inside
BNP were part of this effort, during a brief visit by Alan
Channing. Only two adult Hyperolius benguellensis and
several species of tadpoles were collected (Channing et
al. 2013; A. Channing, pers. comm.), with the material
deposited in Berlin Zoological Museum, and other
Amphib. Reptile Conserv.
of,
observations remained unpublished. More recent surveys
include two short visits to BNP in 2017 and 2018 by
Butler et al. (2019).
To document the herpetofauna of BNP, we conduct-
ed surveys in and around the park from 2015 to 2018
as part of the Southern African Science Service Centre
for Climate Change and Adaptive Land Management
(SASSCAL) project, which established an observa-
tory in BNP. This is part of a network of five other
Angolan observatories, and a total of 47 observatories
throughout Southern Africa (Jurgens et al. 2018). Re-
sults of herpetological surveys in Tundavala observa-
tory, southwestern Angola, were published recently
(Baptista et al. 2018). This paper draws upon records
and photographs of BNP herpetofauna partially avail-
able since 2017 through SASSCAL’s on-line platform
(SASSCAL ObservationNet 2018), and is their first
formal publication. It presents the results of the 2015-—
2018 SASSCAL surveys, and it includes collated data
from recent and historical collections and observations
made by others in and around BNP to provide a more
comprehensive account.
Materials and Methods
Study Area
Bicuar National Park (BNP) in Huila Province,
southwestern Angola, was declared as a Partial Game
Reserve in 1957 to protect populations of big game
before being upgraded to National Park status in 1964
(Teixeira 1968; Huntley et al. 2019a). The park was
originally 790,000 ha in size (Huntley et al. 2019a), with
boundaries described in Diploma Legislativo n° 3527
of 26 December 1964 (Teixeira 1968; Simdes 1971).
In 1972, a governmental decree in Portaria 384/72
deproclaimed areas of northern BNP for the expansion
of the “Capelongo colonial settlement” (“Colonato de
Capelongo”) [L. Verissimo, pers. comm.], defined the
current boundaries of BNP, and decreased the park’s
area to 675,000 ha (Mendelsohn and Mendelsohn 2018;
Huntley et al. 2019a).
BNP lies at ca. 1,200-1,400 m above sea level (asl),
between the Cunene and Caculuvar rivers on wind-
blown Kalahari sands (Mendelsohn and Mendelsohn
2018). This is the most extensive contiguous body of
sand in the world (Leistner 1967) and extends from the
southern African plateau to the Congo basin. The park
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Teles tS a
Fig, 1. Habi
tat types in the study area. (A) Angolan Miombo woodland on Kalahari sands, BNP; (B) Burkea/Baikiaea woodlands,
Carmira Farm; (C) dry grassy wetland (“mulola”) flanked by miombo woodlands (“tunda”), BNP; (D) temporary pan in a “mulola,”
BNP.
is part of the “Lower Cunene” mesological unit (Diniz
2006; Huntley 2019), and is located in a transition
zone from moist to dry savannas. It comprises both the
Angolan Miombo Woodland and Zambezian Baikiaea
Woodland ecoregions, as defined by Burgess et al.
(2004), which are equivalent to the Brachystegia and
South-west Arid biomes, respectively, as characterized
by Huntley (1974). The northern extent is dominated by
miombo woodlands, consisting mostly of Brachystegia
spiciformis and Julbernardia paniculata, while the south
is covered predominantly by savannas dominated by
Burkea africana (Teixeira 1968) [Fig. 1], and Angolan
Mopane woodlands are present to the south of the park
(Huntley 2019). In addition to woodlands, thickets, and
scrublands of varied composition, open drainage lines
hosting grasslands with geoxylic suffrutex shrublands
are common throughout; see Teixeira (1968), Barbosa
(1970), and Chisingui et al. (2018) for further details.
Elliptical in shape, the park is ca. 80 km in diameter
from north to south and ca. 110 km from east to west
(Fig. 2). The climate is seasonal, with precipitation
falling mainly from October to April, and nocturnal frost
occuring frequently in the dry season, especially in June
and July. Meteorological data for BNP observatory are
available from 2015 onwards (SASSCAL WeatherNet
Amphib. Reptile Conserv.
2019). The average annual rainfall varies from ca.
900-950 mm in the northern border and 650-700 mm
in the southern border, and average annual temperatures
vary between ca. 19-20 °C in the north and 22—23 °C
in the south, with values for north and south taken from
Quipungo and Mulondo, respectively, in Mendelsohn
and Mendelsohn (2018).
Topographically BNP is generally flat, interrupted by
relatively parallel drainage lines mostly flowing west to
east (Fig. 2). The park is divided through the center by
a larger depression, called Bicuar, which flows in the
north-south direction and forms part of the Cunene River
catchment (Teixeira 1968). Natural grasslands with
geoxylic suffrutex shrublands occur in drainage lines that
are seasonally filled with water (locally called “mulolas”’)
[Fig. 1D] where cold air accumulates at night during the
dry season. Many of the existing permanent water bodies
in the park are artificial excavations made to attract game
for observation purposes (Simdes 1971). The park’s
elevated regions (locally called “tundas’’) are covered by
woodlands, and are only 30-50 m higher in altitude than
the valleys with grasslands. BNP’s soils are mostly sandy
(Missao de Pedologia de Angola 1959; Teixeira 1968),
and arenosols as defined by Jones et al. (2013), with
rare rocky outcrops. The landscape surrounding BNP
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Handa Farm
Quipungo
Capelongo
Chibemba
Carmira Farm:
14°0'E 15°0'E
i is‘o’s
H— 16°0'S
0 2620 ma.s.l.
— Bicuar National Park boundaries
O Historical records (before 1975)
_ Recent records from Butler et al. (2019)
A Recent records from this study (after 2008)
16°0'E
Fig. 2. Left: Bicuar National Park (BNP) and surveyed sites from historical and recent records. Right: Angola with provincial
boundaries and location of BNP. Source of satellite image: Maxar (https://www.digitalglobe.com/).
is similar (Barbosa 1970; Mendelsohn and Mendelsohn
2018) such that records from localities surrounding the
park are also reported in this work.
Survey Methods and Data Sources
For this study, surveys of herpetofauna were performed
in BNP from October 2015 to April 2018. These included
opportunistic collections during occasional visits to the
park, and two series of focused surveys, from 2-10
December 2016 (during the rains) and 3-7 November
2017 (at the onset of the rains). For both surveys, diurnal
and nocturnal Visual Encounter Surveys (VES) were
performed, as well as dipnetting in water bodies by
scooping the bottom, using nets of varied shape and mesh
size. Trap arrays consisting of drift fences with pitfall and
funnel traps were set during the 2016 survey at three sites
within the following habitats: miombo woodlands not
burnt for more than one year (site T1, see Appendix | for
coordinates and duration), miombo woodlands not burnt
for more than five years (T2, Appendix 1), and grassland
along a drainage line (T3, Appendix 1). Each trap array
consisted of one plastic drift fence (15 m long and 50 cm
high) with two pitfall traps, one at each end of the drift
fence, and six funnel traps placed on adjacent sides of
the fence. Collecting sites in BNP and the surroundings
included the Main Camp and permanent water bodies
(waterhole near the Main Camp, Lagoa da Matemba,
Lagoa do Djimbi, and Lagoa Nougalafa, among others).
These sites are mapped in Fig. 2, and geographic
Amphib. Reptile Conserv.
coordinates are provided in Appendix 1. Surveyed habitat
types included miombo and Burkea/Baikiaea woodlands,
ponds, and excavations in drainage lines where water is
permanently provided by water pumps. Large portions
of the surveyed areas in the north were burnt two to four
weeks prior to being surveyed.
Additional observations include records from
Channing’s 2009 visit (A. Channing, pers. comm.), as
well as opportunistic records from other researchers
working in the region (Manfred Finckh and Francisco
Maiato, who provided photographs), and from two farms
located near the park. Carmira Farm, located ca. 40 km
northeast of Cahama and ca. 46 km south of BNP (site CF),
has staff with a personal interest in collecting reptiles, as
they have created a collection (Fig. 3) comprising snakes,
amphisbaenians, and writhing skinks. Handa Farm, 30
km northwest of Quipungo and 48 km northwest of BNP
(site HF), maintains a collection of photographic records
of its fauna, including reptiles. All recent records in these
sources were considered for this study, and all except
Channing’s 2009 data (A. Channing, pers. comm.) were
verified by the authors. Butler et al. (2019) addressed
BNP herpetofauna, and these results have also been
incorporated into this work.
Collected specimens were photographed and
euthanized by either submersion (in the case of frogs) or
injection into the intracoelomic cavity (for reptiles) of a
solution of tricaine methanesulfonate (MS222) [Conroy
et al. 2009]. Tissue (liver or muscle) was preserved in
99.5% ethanol for genetic analysis. Specimens were fixed
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
\
\
Fig. 3. Carmira Farm private collection.
with formalin, then transferred to water (to remove the
formalin), before finally being transferred to 70% ethanol
for long-term storage. All photographs were taken by the
first author (N. Baptista), except when noted. Specimens
are held in the herpetological collection of Instituto
Superior de Ciéncias da Educacao da Huila (ISCED-
Huila), Lubango, Angola. Additional specimens that
were not collected for this study are deposited in Carmira
Farm’s private collection (Fig. 3).
Field guides (Branch 1998; Schigtz 1999; Channing
2001; Marais 2004; du Preez and Carruthers 2009;
Channing et al. 2012; Channing and Rodel 2019) were
used for species identification, and additional taxon-
specific literature was consulted when necessary.
Nomenclature followed online databases: Amphibian
Species of the World (Frost 2019) for amphibians, and
The Reptile Database (Uetz et al. 2019) for reptiles, and
was updated when appropriate. Only materials from the
ISCED-Huila collection and Carmira and Handa Farms
were examined for this study. Taxonomic identification
of historical records (published in the literature, and
unpublished records from Haacke’s surveys) and acoustic
survey records may require verification.
Localities for historical data compiled for the BNP
region (yellow dots in Fig. 2) were selected based
on distances to the park (1.e., those within a 100 km
radius of the park’s boundaries) and physiographic
similarity (Huntley 2019). The only exception to this
is Humbe, which is located 110 km south of the park,
but was also included in this account since it is an
important historical collection site and is the type
locality of several reptile species. Selected historical
Amphib. Reptile Conserv.
localities were: Cahama and surroundings, Capelongo
(= Kapelongo, = Folgares), Catequero and surroundings,
Chibemba and surroundings, Dongue and surroundings,
Gambos (= Chibemba, see discussion in Branch et
al. [2019a]), Humbe, Humbi (= Humbe), Humbia (=
Humbe), Kandingu (= Kului River), Kangela (= Kului
River), Kului River, Mulondo, Mupa, Osi (= Osse),
Osse, Quipungo, and Viriambundo. Records from these
localities were compiled from published literature such
as Bocage (1895), Monard (1937a,b), Schmidt (1933),
Bogert (1940), Laurent (1964), Gans (1976), Poynton
and Haacke (1993), and from unpublished information
in the Ditsong (=Transvaal) National Museum of Natural
History's database (Haacke, TM).
Collected data were grouped into three classes (Fig.
2): 1) historical records collected before 1975, which
include records published in historical literature and
unpublished records from TM; 11) recent records from
Butler et al. (2019); and 11) recent records from this
study, which refer to either data collected during field
surveys from 2009 onwards performed within the
scope of the SASSCAL project, A. Channing’s personal
records, opportunistic photographic records collected by
other researchers in the region, and records from Carmira
Farm and Handa Farm.
Results
The combined records (published and unpublished, recent
and historical) of herpetofauna biodiversity from the
BNP region comprises a total of 94 taxa. This includes 21
amphibian taxa (Table 1) and 73 reptilian taxa (36 lizards,
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Table 1. Amphibians recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and recent
records. Type of record: C = advertisement call; L = literature; O = observation; P = photograph; RR = new record for the region; V
= voucher. Period of record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species
citations may occur under different names.
10.
11.
12.
13.
14.
es:
16.
17.
18.
Species
Arthroleptidae
Leptopelis bocagii (Gunther, 1865)
Bufonidae
Mertensophryne aff. mocquardi (Angel, 1924)
Sclerophrys poweri (Hewitt, 1935)
Sclerophrys pusilla (Mertens, 1937)
Sclerophrys regularis (Reuss, 1833)
Hemisotidae
Hemisus cf. guineensis Cope, 1865
Hyperoliidae
Hyperolius angolensis Steindachner, 1867
complex
Hyperolius benguellensis (Bocage, 1893) complex
Kassina senegalensis (Duméril and Bibron 1841)
Microhylidae
Phrynomantis bifasciatus (Smith, 1847)
Phrynobatrachidae
Phrynobatrachus mababiensis FitzSimons, 1932
Phrynobatrachus natalensis (Smith, 1849)
Pipidae
Xenopus petersii Bocage, 1895
Ptychadenidae
Hildebrandtia cf. ornata (Peters, 1878)
Ptychadena ansorgii (Boulenger, 1905)
Ptychadena oxyrhynchus (Smith, 1849)
Ptychadena porosissima (Steindachner, 1867)
Pyxicephalidae
Pyxicephalus adspersus Tschudi, 1838
Amphib. Reptile Conserv.
Type of
record
RR, V
RR, V
Lev.
je
>
Le @
101
Records in the region of BNP _ Inside
Locality (Reference) BNP?
BNP (this study) Y
Mulondo (Monard 1937a)
BNP (this study)
Capelongo (Butler et al. 2019);
BNP (this study)
Humbe, Mulondo, Mupa, Osi (=
Osse) (Monard 1937a)
4
BNP (this study) Y
Capelongo, Osi (= Osse)
(Monard 1937a); BNP (Butler et Y
al. 2019; this study)
BNP (Channing et al. 2013);
BNP (Butler et al. 2019; this Y
study)
Mulondo (Monard 1937a); BNP Y
(this study)
Mulondo (Monard 1937a); BNP Y
(this study)
BNP (Butler et al. 2019; this Y
study)
Kangela (Monard 1937a); BNP Y
(this study)
Kandingu, Osi (= Osse)
(Monard 1937a); BNP (Butler et Y
al. 2019; this study)
Mulondo, Osi (= Osse) (Monard
1937a); Dongue (Poynton
and Haacke 1993); between
Chibemba and Cahama (this
study)
Kandingu (Monard 1937a)
Osi (= Osse) (Monard 1937a);
BNP (Butler et al. 2019; this Y
study)
BNP (this study) Y
Humbe (Bocage 1895); Carmira
Farm (this study)
Period of
record
A
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Table 1 (continued). Amphibians recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical
and recent records. Type of record: C = advertisement call; L = literature; O = observation; P = photograph; RR = new record for
the region; V = voucher. Period of record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore
original species citations may occur under different names.
Rrecics Type of Recordsinthe regionof BNP Inside Period of
P record Locality (Reference) BNP? record
BNP (Butler et al. 2019;
19. Tomopterna ahli (Deckert, 1938) Channing and Becker 2019) iG A
Catequero (Boulenger 1907);
, Calequero (= Catequero), 2 km
20. Tomopterna cf. cryptotis (Boulenger, 1907) Celery NW of (Poynton and Haacke ¥ A,B
1993); BNP (this study)
21. Tomopterna tuberculosa (Boulenger, 1882) BNP (Butler et al. 2019) 4 A
32 snakes, four testudines, and one crocodilian, Table 2).
Many of Haacke’s data represent new records for the
region (see Table 2), highlighting the relevance of his
collections. The recent records resulting from this study
recorded a total of 53 taxa; 16 amphibian taxa distributed
across nine families and 13 genera (Table 1), and 36
reptilian taxa (15 lizards, 18 snakes, two testudines, and
one crocodilian) distributed among 17 families and 35
genera (Table 2). This study revealed the first record
of Xenocalamus bicolor bicolor, the second records of
Sclerophrys poweri and of Amblyodipsas ventrimaculata
(together with the record of Butler et al. [2019]), and
the fourth record of Monopeltis infuscata in Angola. In
total, 89 specimens were collected and deposited in the
herpetological collection of ISCED-Huila.
Comments on the recent records from this study
are provided in the species accounts below, which are
arranged alphabetically by class, family, genus, and
species, with notes on taxonomy and the relevance
of the discoveries. For each species, the material used
is described as the type of record, the field number of
the collected specimen when applicable, and a code in
brackets which represents the site where the specimen
was recorded (see Appendix 1). Some records could
not be assigned to a species with certainty because no
voucher specimens were available for verification (e.g.,
Hildebrandtia, Afrotyphlops), or due to taxonomical
uncertainty in the group to which they belong (e.g.,
Hyperolius, Hemisus, Panaspis). In these cases, the
nomenclature followed Sigovini et al. (2016). Collected
tadpoles were not identified and are therefore not listed
as materials below, and their future identification awaits
the results of DNA sequencing. The only exceptions to
this exclusion are the tadpoles assigned to Kassina.
Species Accounts
Amphibia
Arthroleptidae
Leptopelis bocagii (Gunther, 1865)
Bocage's Burrowing Treefrog (Fig. 4A—B)
Amphib. Reptile Conserv.
Material: NB520 (30); NB546 (28); NB547 (29);
NB710 (27); NB765 (27); NB766 (27).
Comment: Reported in several localities in Angola
(Ceriaco et al. 2018c; Marques et al. 2018), including
recent records from Huila Province (Baptista et al. 2018).
It is considered a complex of cryptic species (Schiotz
1999), and the Angolan material assigned to Hylambates
angolensis Bocage, 1893, currently in the synonymy of
L. bocagii, requires further study (Perret 1976). Dorsal
coloration of individuals in BNP varied from completely
La]
= . % , r ‘ * ‘ad a } + : is LA ’ “ of tye ne st
Fig. 4. Leptopelis bocagii, BNP. (A) female with plain back;
(B) male with blotch in back.
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
plain to black with a horseshoe shaped blotch with white
dots in the back (Fig. 4A—B).
Bufonidae
Sclerophrys poweri (Hewitt, 1935)
Western Olive Toad (Fig. 5)
Material: NB512 (36); NB756 (25); NB764 (26);
NB767 (26); NB768 (26); NB769 (26).
Comment: Also occurring in northern Namibia and
Botswana (Channing 2001), this is the second confirmed
record of the species for Angola, after a previous record
near Calai (Conradie et al. 2016). Some early records
of Bufo regularis sensu latu may also refer to S. poweri
(Ruas 1996). Bufo regularis humbensis Monard, 1937
was originally described from Mulondo, close to BNP.
It is currently placed under the synonymy of S. garmani
(Tandy and Keith 1972), which in Angola refers to
S. poweri, and this synonymy should be reviewed.
Sclerophrys poweri is very abundant in BNP and was
found hundreds of meters away from water on moist
nights. Breeding was observed in permanent pans, with
males calling in choruses at night and eggs typically laid
in gelatinous single strings.
Sclerophrys pusilla (Mertens, 1937)
Southern Flat-backed Toad (Fig. 6)
Material: NB056 (31); NB763 (26).
Comment: Taxonomy and identification of bufonids
in Angola remains problematic (Baptista et al. 2019).
Sclerophrys pusilla represents populations previously
assigned to S. maculata in eastern and southern Africa,
including Angola (Poynton et al. 2016). This species is
known from several localities in the country (Poynton
and Haacke 1993; Ruas 1996, 2002; Conradie et al.
2016; Ceriaco et al. 2018c; Marques et al. 2018). It
was heard calling in BNP on 24 January 2009, but not
collected (A. Channing, pers. comm.), and was recently
recorded from Capelongo, near BNP (Butler et al. 2019).
It was also found around the Main Camp facilities and in
a permanent water body.
Hemisotidae
Hemisus cf. guineensis Cope, 1865
Guinea Snout-burrower (Fig. 7A—C)
Material: NB511 (15); NB550 (T2); NB551 (T2).
Comment: Tadpoles of this species were collected
in BNP during the 2009 survey (A. Channing, pers.
comm.). The taxonomy of Hemisus guineensis and H.
marmoratus is not fully resolved. Angolan specimens of
both species have been treated as a single taxon in the
past (Hemisus guineensis microps Laurent, 1972) and
records of the genus are scattered throughout the country
(Ruas 1996; Marques et al. 2018). Recent records of
Hemisus from Cangandala have been considered as H.
guineensis (Ceriaco et al. 2018c; Vaz Pinto and Baptista,
Amphib. Reptile Conserv.
unpub. data). Coloration of adult frogs from BNP ranges
from finely spotted forming lines, and mottled forming
continuous blotches to almost plain with very small
spots (see Fig. 7A—C). A similar pattern of variation in
coloration was reported by W. Conradie (pers. comm.)
in southeastern Angola, with all forms genetically
confirmed as being H. cf. guineensis. Based on this, and
the proximity to a previous record from the Cubango
basin (Monard 1937a), BNP specimens likely belong to
the same taxon.
Hyperoliidae
Hyperolius angolensis Steindachner, 1867 complex
Angola Reed Frog
Material: NB523 (41); NB524 (41); NB538 (27);
NB539 (27); NB540 (27); NB541 (27).
Comment: This species was heard calling in BNP (site
31) on 24 January 2009, but no material was collected
(A. Channing, pers. comm.). It was recently recorded
in BNP by Butler et al. (2019), who provided photos of
coloration variations. This is another unresolved complex
of reed frogs in Africa (see Schigtz 1999), with a number
of names available for Angolan populations (Baptista et
al. 2019, as H. parallelus). In Angola, this complex is
recorded throughout the country (Monard 1937a; Laurent
1950, 1954, 1964; Poynton and Haacke 1993; Conradie
et al. 2016; Baptista et al. 2018; Ceriaco et al. 2018c;
Marques et al. 2018), with consistent regional color
patterns. Poynton and Haacke (1993) referred to previous
records in Huila Province as Hyperolius marmoratus
huillensis.
Hyperolius benguellensis (Bocage, 1893) complex
Benguela Long Reed Frog (Fig. 8A—B)
Material: NB510 (36); NB526 (41); NB542 (27);
NB543 (27); NB544 (27).
ZMB 77273; ZMB 77274 (collected by Alan Channing,
not analyzed).
Comment: Hyperolius benguellensis belongs to the
challenging Hyperolius nasutus complex, with a
problematic taxonomy throughout Africa (Schiotz 1999;
Amiet 2005; Marques et al. 2018). Channing et al.
(2013) proposed a rearrangement for this group based on
morphology, genetics, and advertisement calls, resulting
in four species occurring in Angola: H. nasutus, H.
dartevellei, H. adspersus, and H. benguellensis. Of these,
three were originally described from Angola: Hyperolius
nasutus Gunther, 1865, type locality: Duque de Braganca
(= Calandula); HAyperolius adspersus Peters, 1877,
type locality: Chinchoxo, in Cabinda; and Hyperolius
benguellensis (Bocage, 1893) type locality: "Cahata" that
has been incorrectly assigned to Caota (e.g., Channing
2001; Marques et al. 2018; Frost 2019). In fact, Cahata
is located 5 km east of Balombo Municipality and was
a known collecting site for the famous naturalist José
de Anchieta in the nineteenth century (Bocage 1895).
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
vad ‘ pty.
aS,
a 2 tle. rly
rophrys pusilla, BNP
Sele
ae .
Fig. 6.
Although the region is still located in Benguela Province,
it lies on the plateau at 1,230 m asl, more than 400 km
east of the coastal town of Benguela and closer to the
town of Huambo, while Caota is found on the outskirts
of Benguela at 20 m asl. The name “benguellensis” is
therefore misleading, and is probably the reason why
Cahata was confused with Caota, but the latter is a beach
site in the semi-arid Angolan southwest, and an unlikely
habitat for a reed frog. We therefore re-establish the type
locality of H. benguellensis to Cahata, near Balombo. The
assignment of erroneous names to Angolan localities has
been detected in other cases (Branch et al. 2017, 2018;
Vaz Pinto et al. 2019), thus special attention must be given
to this when consulting historical and recent literature.
Channing et al. (2013) assigned one specimen from BNP
to H. benguellensis, and we assign these specimens to this
name, with the altitude similar to the true type locality
providing further support. Butler et al. (2019) collected
one specimen from BNP, recording it as H. cf. nasutus,
and in this study we tentatively regard this record as
the same as ours. Both species, H. benguellensis and H.
nasutus, are sympatric in Cangandala National Park (Vaz
Pinto, unpub. data). Specimens from this group have been
also found in western Zambia (Bittencourt-Silva 2019)
and assigned to H. dartevellei and H. nasicus. Similar to
H. angolensis complex, a more complete understanding
of this complex in Angola requires countrywide surveys
and an integrated analysis of molecular, morphological,
and advertisement call data.
Kassina senegalensis (Dumeéril and Bibron, 1841)
Bubbling Kassina
Material: NB525 (T1); NB536 (tadpoles) (7); NB545
(T3); NB552 (T2); NB761 (26).
Comment: Widespread throughout Africa and in Angola
(Baptista et al. 2018; Marques et al. 2018). This species
has been previously recorded in BNP as tadpoles (A.
Channing, pers. comm.). Although subspecies have
been proposed based on color patterns (Laurent 1957),
more comprehensive studies are required to resolve this
species’ taxonomy.
- Saeed 4 ~ 3 Pr = ss im) 7 a oes!
Fig. 7. Hemisus cf. guineensis, BNP. (A—C) Three variations
in coloration.
Amphib. Reptile Conserv. 104 December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 8. Hyperolius benguellensis complex, BNP. (A) Ventral
view; (B) dorsal view.
Microhylidae
Phrynomantis bifasciatus (Smith, 1847)
Banded Rubber Frog
Comment: This species was heard calling in BNP (site
31) on 24 January 2009, but no material was collected
(A. Channing, pers. comm. ). In Angola, it is known from
Mulondo (Monard 1937a), which is located near the
boundary of BNP, in addition to Quissange and Benguela
(Bocage 1895), and Chingo (Ferreira 1904).
Phrynobatrachidae
Phrynobatrachus mababiensis FitzSimons, 1932
Mababe Puddle Frog
Comment: This species was heard calling in BNP
(site 31) on 24 January 2009, and a single tadpole (A.
Channing, pers. comm.) and adults (Butler et al. 2019)
have been collected in BNP. In Angola, it is recorded
from Lagoa Nuntechite (Poynton and Haacke 1993),
Cubango, Cuito and Cuando rivers basins (Conradie
et al. 2016), and Tundavala (Baptista et al. 2018). This
species belongs to the P. cryptotis group (Marques et al.
2018) and is in need of further taxonomic studies all over
Africa (Zimkus et al. 2010).
Amphib. Reptile Conserv.
Phrynobatrachus natalensis (Smith, 1849)
Snoring Puddle Frog
Comment: This species was heard, but not recorded,
calling in BNP (site 31) on 24 January 2009; no
material was collected (A. Channing, pers. comm.). It is
widespread in Angola (Ruas 1996, 2002; Marques et al.
2018) and includes several cryptic taxa (Zimkus et al.
2010) that are presently being investigated. Additional
specimens collected from BNP will be crucial for species
confirmation.
Pipidae
Xenopus petersii Bocage, 1895
Peters' Clawed Frog
Material: NB757 (27); NB758 (27); NB759 (27).
Comment: This species is widespread in Angola
(Monard 1937a as_X. laevis, Ruas 1996, 2002; Baptista
et al. 2018; Ceriaco et al. 2018c; Marques et al. 2018). It
has been previously recorded in BNP from both tadpoles
(A. Channing, pers. comm.) and adults (Butler et al.
2019). Furman et al. (2015) consider that in Angola,
X. petersii is widespread and X. poweri is restricted to
southeastern Angola, but few samples from Angola were
used in their analysis and this genus is worthy of a more
comprehensive assessment in the country. Hamerkop
(Scopus umbretta) and Lilac-breasted Roller (Coracias
caudatus) were seen preying upon this species in BNP.
Ptychadenidae
Hildebrandtia cf. ornata (Peters, 1878)
Ornate Frog (Fig. 9)
Material: Photographic record (F. Maiato, on wetland
between Chibemba and Cahama, approximate
coordinates same as site 42).
Comment: Two species of Hildebrandtia exist in Angola:
H. ornata and H. ornatissima (Marques et al. 2018;
Baptista et al. 2019). Hildebrantia ornata is limited to the
southwest, and H. ornatissima extends northwards to the
central plateau (Ruas 1996; Marques etal. 2018). Boulenger
(1919) provides morphological distinction between H.
ornatissima (Bocage, 1897), endemic to Angola, and H.
ornata (Peters, 1878) (= R. ruddi), originally described
from Kenya but with a wide distribution in Africa. Perret
(1976) considered H. ornata and H. ornatissima as two
valid species based on morphology, but Poynton and
Haacke (1993) contest that, and consider them subspecies.”
Specimens collected from Dongue, 28 km west of BNP
and other localities in southwestern Angola had mixed
features from both taxa and were assigned to H. ornata
ornata (Poynton and Haacke 1993). A single frog was
photographed, approximately 55 km southwest of BNP’s
boundaries, and it is provisionally assigned to H. ornata
based on the identification of material collected in close
proximity (Poynton and Haacke 1993). Hildebrandtia
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
-
Pris.
ta, between Chibemba_ and
‘A (
Fig. 9. Hildebrandtia cf. orn
Cahama (Photo by F- Maiato).
a
specimens have also been recently collected from several
localities in Huila and Malanje provinces (Baptista and
Vaz Pinto, unpub. data), and the genus requires a revision
in the country.
Ptychadena oxyrhynchus (Smith, 1849)
Sharp-nosed Ridged Frog (Fig. 1OA—B)
Material: NB750 (25).
Comment: Species identification for Ptychadena in
Angola is not resolved (Baptista et al. 2019). A single
specimen was found near Lagoa da Matemba, but no
advertisement call was heard. It was assigned to P.
oxyrhynchus based on morphology and coloration (Fig.
10A-B). This species has recently been recorded from
BNP (Butler et al. 2019) and is known from several
localities in Angola (Marques et al. 2018).
Ptychadena porosissima (Steindachner, 1867)
Grassland Ridged Frog
Comment: This species was heard calling in BNP (site 31)
on 24 January 2009, but no material was collected and no
call was recorded (A. Channing, pers. comm.). Widespread
in sub-Saharan Africa, and recorded in Angola from the
west and the northeast (Ruas 1996; Marques et al. 2018).
Additional specimens will be important for confirmation
of species identification in BNP.
Pyxicephalidae
Pyxicephalus adspersus Tschudi, 1838
African Bullfrog
Material: Interviews.
Comment: Staff from Carmira Farm mentioned that
this frog—which is unmistakable by its distinctive size,
morphology, and behavior—appears during the first
Amphib. Reptile Conserv.
heavy rains. Pyxicephalus adspersus is recorded from
southern Angola in Humbe (Bocage 1895), Mupanda
(Monard 1937a), and Pereira d’E¢a (= Ondjiva) and 23
km NW Pereira d’Eca (Poynton and Haacke 1993, as P.
a. edulis). Several synonymies exist within P. adspersus
(Frost 2019). Consensus regarding whether P. edulis
occurs in the Zambezi Region (previously the Caprivi
Strip), has not been reached (Herrmann and Branch
2013), and the Angolan material requires further analysis.
Locally called “mafuma,” it 1s captured for consumption
and bushmeat trade. It may also have cultural relevance
in Angola, as in some parts of Cunene Province this
frog’s mating behavior is said to inspire a traditional fight
called “engolo” among the Nkhumbi people (J. Moniz,
pers. comm. ).
Tomopterna cf. cryptotis (Boulenger, 1907)
Cryptic Sand Frog (Fig. 11 A—C)
Material: NB751 (25); NB752 (25); NB753 (25);
NB754 (25); NB755 (25); NB762 (26).
Comment: The species was found breeding in early
December, with males calling in loud choruses on
banks of water bodies in BNP. Collected specimens
had considerable coloration variation (see Fig. 11A—C).
Tomopterna cryptotis was originally described from
Catequero (ca. 95 km south of BNP), and has been
recorded between Calequero (= Catequero) and Cahama
(ca. 75 km southwest of BNP) [Poynton and Haacke
1993] among other localities in Angola (Ruas 1996;
Marques et al. 2018). This species is morphologically
indistinguishable from 7’ tandyi (Channing and Bogart
1996), which was originally described from the Eastern
Cape in South Africa and is known from Namibia,
Botswana, and South Africa (Channing 2001, du Preez
and Carruthers 2009). Although 7° tandyi is considered
as being present in southwestern Angola (Channing 2001;
Channing and Rodel 2019), there are no literature records
from the country, and its occurrence is presumably based
on the morphology of similar frogs in Namibia (A.
Channing, pers. comm.). However, 7Zomopterna species
are highly cryptic, and difficult to distinguish based on
morphology. Due to the fact that the BNP records are near-
topotypical, these specimens are assigned to 7’ cryptotis,
but the advertisemen calls heard in BNP resembled
those of 7? tandyi provided by du Preez and Carruthers
(2019). Further integrative revision of these species in
Angola is needed to confirm this assignment. Two other
species from the same genus have recently been recorded
from BNP (Butler et al. 2019): 7 tuberculosa and T.
damarensis, which was recently re-assigned to 7ompterna
ahli (Channing and Becker 2019), which means that at
least three species may occur sympatrically. Given
the highly cryptic morphology of species within this
genus (Channing and Rodel 2019), and the continuing
descriptions of new species (Wilson and Channing 2019),
all of these new records require revision.
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 10. P
detail of thighs.
Reptilia
Squamata
Sauria
Agamidae
Acanthocercus sp.
Tree Agama (Fig. 12)
Material: NB709 (31).
Comment: This species was previously assigned to
Acanthocercus atricollis (Smith, 1849) until Wagner
et al. (2018) revived the name A. cyanocephalus for
western populations, which included Angola. Reported
in several publications from Angola (Bocage 1879, 1895;
Ferreira 1902; Boulenger 1905; Monard 1931, 1937b;
Schmidt 1933; Laurent 1950, 1964; Manacas 1963;
Conradie et al. 2016; Ceriaco et al. 2018c; Marques et
al. 2018), but material from Huila Province belongs
to a different species, which is in the process of being
described (Marques et al. 2018; Butler et al. 2019).
Recently recorded in BNP (Butler et al. 2019), abundant
at the park’s headquarters, and found on large and tall
Burkea africana trees.
Agama aculeata (Merrem, 1820)
Ground Agama
Material: NB770 (32).
Comment: Ground Agamas occur widely in southern
Africa (Bates et al. 2014) and are reported throughout
Angola (Marques et al. 2018). The taxonomy of Angolan
populations remains unresolved, and a recent phylogeny
of Agama (Leaché et al. 2014) did not include Angolan
Amphib. Reptile Conserv.
ra P B > © Te
a Ce a ee
Fig. 11. Zomopterna cf. cryptotis, BNP. (A—C) Three variations
in coloration.
samples. Recently recorded in BNP (Butler et al. 2019),
in this study it was found on the ground in degraded
shrubland in the outskirts of BNP.
Amphisbaenidae
Monopeltis cf. anchietae (Bocage, 1873)
Anchieta's Spade-snouted Worm Lizard (Fig. 13)
Material: One photographic record of a freshly killed
individual (L. Gata, CF).
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Table 2. Reptiles recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and recent records.
Type of record: CR = new record for the country; H = unpublished record from Ditsong (= Transvaal) Museum’s collection; L =
literature; O = observation; P = photograph; RR = new record for the region; V = voucher; E = endemic. Period of record: A =
after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species nomenclature may occur under
different names.
10.
11.
12:
13.
14.
13:
Taxa
Sauria
Agamidae
Acanthocercus sp.
Agama aculeata (Merrem, 1820)
Agama planiceps shacki Mertens, 1938
Amphisbaenidae
Monopeltis cf. anchietae (Bocage, 1873)
Monopeltis infuscata Broadley, 1997
Monopeltis perplexus Gans, 1976
Zygaspis quadrifrons (Peters, 1862)
Chamaeleonidae
Chamaeleo dilepis quilensis (Bocage
1886)
Cordylidae
Cordylus machadoi Laurent, 1964
Gekkonidae
Chondrodactylus fitzsimonsi (Loveridge,
1947)
Chondrodactylus laevigatus (Fischer,
1888)
Hemidactylus benguellensis Bocage, 1893
Lygodactylus angolensis Bocage, 1896
Lygodactylus bradfieldi Hewitt, 1932
Pachydactylus punctatus Peters, 1854
complex
Amphib. Reptile Conserv.
Endemic?
Ee
Type of
record
mbt Bs
H,L,V
LEN:
108
Records in the region
of BNP Inside Period of
Locality (and BNP? record
Reference)
Mupa (Monard 1937b);
BNP (Butler et al. 2019; Yi A,B
this study)
Cahama and Chibemba,
21 km NW of (Haacke,
TM); BNP (Butler et al. y
2019; this study)
Chibemba, 5 km S;
Dongue, 10 km NW of A,B
(Haacke, TM)
Humbe (Bocage 1873);
Mupa (Monard 1937b); A,B
Carmira Farm (this study)
Humbe (Bocage 1873;
Broadley 1997); Carmira A,B
Farm (this study)
Humbe (Gans 1976) B
BNP (Butler et al. 2019);
Carmira Farm (this study) :
Cahama, 23 km SE
(Haacke, TM); Kului
(Monard 1937b); BNP Y A,B
(Butler et al. 2019; this
study)
Chibemba, 5 km S;
Humbia, 12 km E B
(Haacke, TM)
Viriambundo (Haacke,
TM)
Mulondo (Schmidt 1933);
Humbe (Monard 1937b);
BNP (Butler et al. 2019); ;
Carmira Farm (this study)
Capelongo (Butler et al.
2019)
BNP (this study) Y
Humbe-Cahama, 36 km
from; Humbe, 5 km N of;
Humbia (Haacke, TM); é
BNP (Butler et al. 2019)
Kului (Monard 1937b;
Bauer et al. 2006); BNP yy A,B
(this study)
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Table 2 (continued). Reptiles recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and
recent records. Type of record: CR = new record for the country; H = unpublished record from Ditsong (= Transvaal) Museum’s
collection; L = literature; O = observation; P = photograph; RR = new record for the region; V = voucher; E = endemic. Period of
record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species nomenclature may
occur under different names.
Records in the region
; Type of of BNP Inside Period of
9
US pens record Locality (and BNP? record
Reference)
Rhoptropus barnardi Hewitt, 1962 eek a eee
He: H, RR Humbia, 12 km E B
(Haacke, TM)
Gerrhosauridae
Capelongo, Mulondo
(Monard 1937b);
Gerrhosaurus bulsi-multilineatus complex pees Bs ae Pee
17. E* Hale Weck es ee Y A,B
me ¥. Chibemba, Cahama, 30 °
km SE of (Haacke, TM);
BNP (Butler et al. 2019;
this study)
Dongue, 10 km NW of
18. Matobosaurus maltzahni (De Grys, 1938) H, RR (Haacke, TM) B
Lacertidae
Mulondo (Monard
19. Heliobolus lugubris (Smith, 1838) H, L 1937b); Cahama, 3 km B
NW of (Haacke, TM)
20. Ichnotropis bivittata Bocage, 1866 L Kului (Monard 1937b)
BNP (Butler et al. 2019;
21. Ichnotropis capensis (Smith, 1838) LIV this study) A
22. Meroles squamulosus (Peters, 1854) |B CapelongoMonard B
1937b)
3 Nucras broadleyi Branch, Conradie, Vaz E L Capelongo (Monard B
’ Pinto, Tolley 2019 1937b)
Scincidae
24. Acontias occidentalis FitzSimons, 1941 L pipe (Monaro:
FitzSimons 1941)
25. Mochlus sundevalli (Smith, 1849) RR, V_— Carmira Farm (this study)
; a Bare BNP (Butler et al. 2019;
26. Panaspis wahlbergi-maculicollis complex | es this study) nA
Chibemba (Laurent
27. Sepsina angolensis Bocage, 1866 | ae 1964); Viriambundo B
(Haacke, TM)
28. Trachylepis albopunctata (Bocage, 1867) L BNP (Butler et al. 2019) Y A
Mupa (Monard 1937b);
ae: Chibemba, 11 km S;
29. Trachylepis binotata (Bocage, 1867) Hi Ts Humbe (Haacke, TM): wg A,B
BNP (Butler et al. 2019)
Humbe (Schmidt 1933);
30. Trachylepis chimbana (Boulenger, 1887) H Humbia, 12 km E of B
(Haacke, TM)
Humbe to Cahama, 36
PyOA 2e km NW of (Haacke,
31. Trachylepis spilogaster (Peters, 1882) H, L, V TM): BNP (Butler et al. Y A,B
2019; this study)
Trachylepis sulcata ansorgii (Boulenger, Chibemba, 11 km S
32 4907) H, RR (Haacke, TM) :
Amphib. Reptile Conserv. 109 December 2019 | Volume 13 | Number 2 | e203
Table 2 (continued). Reptiles recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and
recent records. Type of record: CR = new record for the country; H = unpublished record from Ditsong (= Transvaal) Museum’s
collection; L = literature; O = observation; P = photograph; RR = new record for the region; V = voucher; E = endemic. Period of
record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species nomenclature may
Herpetofauna of Bicuar National Park, Angola
occur under different names.
ao!
34.
oot
36.
aM.
38.
39.
40.
4].
42.
43,
44,
45.
46.
Taxa
Trachylepis sulcata sulcata (Peters, 1867)
Trachylepis varia (Peters, 1867) clade B
(Weinell and Bauer 2018)
Trachylepis wahlbergi (Peters, 1869)
Varanidae
Varanus albigularis angolensis Schmidt,
1933
Serpentes
Colubridae
Crotaphopeltis hotamboeia (Laurenti,
1768)
Dasypeltis scabra (Linnaeus, 1758)
Dispholidus typus viridis (Smith, 1838)
Philothamnus angolensis Bocage, 1882
Philothamnus semivariegatus (Smith,
1840) sensu lato
Telescopus semiannulatus polystictus
Mertens, 1954
Thelotornis capensis oatesi (Gunther,
1881)
Elapidae
Dendroaspis polylepis Gunther, 1864
Elapsoidea semiannulata semiannulata
Bocage, 1882
Naja anchietae Bocage, 1879
Amphib. Reptile Conserv.
Type of
record
110
Le
oy
L,V
LV.
Records in the region
of BNP
Locality (and
Reference)
Capelongo (Butler et al.
2019)
Capelongo (Monard
1937b); Cahama, 21
km NW — Chibemba,
Humbia, 12 km E of
(Haacke, TM)
Humbi, Capelongo,
Kulu, Mulondo, Mupa
(Monard 1937b); Humbe,
5 km N of (Haacke, TM)
Mulondo, Mupa (Monard
1937b); BNP (this study)
Gambos, Humbe (Bocage
1895); Capelongo
(Monard 1937b);
Nougalafa Lake (this
study)
Gambos (Bocage 1895)
Humbe (Bocage 1895);
Mupa (Monard 1937b);
Capelongo (Bogert
1940); Carmira Farm
(this study)
Capelongo (Bogert
1940); Humbe (Haacke,
TM)
Humbe (Bocage 1895);
Mupa (Monard 1937b),;;
Carmira Farm, Handa
Farm (this study)
Humbe, Gambos (Bocage
1895)
BNP (this study)
Mulondo (Schmidt
1933); BNP, Handa Farm
(this study)
Gambos (Bocage 1895;
Broadley 1998)
Humbe (Bocage 1895);
Capelongo (Bogert
1940); Mupa (Monard
1937b); BNP, Handa
Farm (this study)
December 2019 | Volume 13 | Number 2 | e203
Period of
record
A
oy
)
Baptista et al.
Table 2 (continued). Reptiles recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and
recent records. Type of record: CR = new record for the country; H = unpublished record from Ditsong (= Transvaal) Museum’s
collection; L = literature; O = observation; P = photograph; RR = new record for the region; V = voucher; E = endemic. Period of
record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species nomenclature may
occur under different names.
47.
48.
49.
50.
51.
a2:
53.
54.
53:
56.
57.
58.
bee
60.
61.
62.
63.
Taxa
Naja nigricollis Reinhardt, 1843
Lamprophiidae
Amblyodipsas polylepis (Bocage, 1873)
Amblyodipsas ventrimaculata (Roux,
1907)
Aparallactus capensis Smith, 1849
Boaedon angolensis Bocage, 1895
Hemirhagerrhis viperina (Bocage, 1873)
Prosymna angolensis Boulenger, 1915
Prosymna visseri Fitzsimons, 1959
Psammophis angolensis (Bocage, 1872)
Psammophis mossambicus Peters, 1882
Psammophis subtaeniatus Peters, 1882
Psammophylax tritaeniatus (Gunther,
1868)
Psammophylax ocellatus (Bocage, 1873)
Pseudaspis cana (Linnaeus, 1758)
Xenocalamus bicolor bicolor Gunther,
1868
Leptotyphlopidae
Leptotyphlops scutifrons (Peters, 1854)
Namibiana aff. rostrata (Bocage, 1886)
Amphib. Reptile Conserv.
Type of
record
| gf
2
L,PV
L,V
111
Records in the region
of BNP
Locality (and
Reference)
Humbe (Bocage 1895);
Capelongo (Bogert
1940); Osi (= Osse)
(Monard 1937b); Handa
Farm (this study)
Humbe (Bocage 1895)
BNP (Butler et al. 2019;
this study)
Gambos (Bocage 1895)
Cahama, 3 km NW of
(Haacke, TM); BNP
(Butler et al. 2019);
Carmira Farm (this study)
Humbe (Bocage 1895);
Chibemba, 5 km S
(Haacke, TM)
Capelongo (Bogert
1940); BNP (this study)
Chibemba, 5 km S
(Haacke, TM)
Humbe (Bocage 1895;
Schmidt 1933)
Capelongo (Bogert
1940); Mupa (Monard
1937b); BNP, Handa
Farm (this study)
Humbe, Mulondo, Mupa
(Monard 1937b); BNP
(Butler et al. 2019);
Carmira Farm (this study)
Gambos, Humbe
(Monard 1937b),;
Capelongo (Bogert
1940); Humbe—Cahama,
36 km NW of (Hacke,
TM)
Gambos, Humbe (Bocage
1895; Branch et al.
2019a)
BNP (Butler et al. 2019);
Carmira Farm (this study)
Carmira Farm (this study)
Capelongo (Monard
1937b); Quipungo
(Haacke, TM)
Humbe (Bocage 1895);
BNP (Butler et al. 2019);
Handa Farm (this study)
Inside Period of
BNP? record
A,B
ne A
Y A,B
B
yy B
B
B
Y B
Y: A,B
B
A,B
Ne A
A
B
Y A,B
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Table 2 (continued). Reptiles recorded from inside and the surroundings of Bicuar National Park, Angola, based on historical and
recent records. Type of record: CR = new record for the country; H = unpublished record from Ditsong (= Transvaal) Museum’s
collection; L = literature; O = observation; P = photograph; RR = new record for the region; V = voucher; E = endemic. Period of
record: A = after 2008; B = before 1975. Taxonomy has been updated over the years, therefore original species nomenclature may
occur under different names.
Taxa Endemic?
Pythonidae
64. Python anchietae Bocage, 1887
65. Python natalensis Smith, 1840
Typhlopidae
Afrotyphlops cf. schlegelii (Bianconi,
1849)
Viperidae
66.
67. Bitis arietans Merrem, 1820
68. Causus rhombeatus (Lichtenstein, 1823)
Testudines
Pelomedusidae
69. Pelomedusa subrufa (Bonnaterre, 1789)
70. Pelusios cf. nanus Laurent, 1956
Testudinidae
71. Kinixys cf. belliana Gray, 1831
72. Stigmochelys pardalis (Bell, 1828)
Crocodilia
Crocodylidae
73. Crocodylus niloticus Laurenti, 1768
Comment: Monopeltis anchietae is recorded from
southwestern Angola (Marques et al. 2018), and Branch
et al. (2019b) discuss its taxonomical history. The
coloration pattern of the specimen (Fig. 13) conforms to
the most common pattern associated with M. anchietae
(Broadley et al. 1976), but the photograph resolution
does not allow for the detailed scale counts necessary
to provide a positive identification. The species was
recorded in Humbe (Bocage 1873), approximately 110
km south of BNP, and the Carmira Farm specimen is
provisionally assigned to M. anchietae, pending the
collection of additional material for confirmation.
Monopeltis infuscata Broadley, 1997
Infuscate Spade-snouted Worm Lizard (Fig. 14)
Material: One unlabelled and bleached specimen in
Carmira Farm’s private collection.
Amphib. Reptile Conserv.
TAZ
Records in the region
Type of of BNP Inside Period of
record Locality (and BNP? record
Reference)
Viriambundo (Haacke,
H, RR TM) B
Capelongo (Bogert
L,V 1940); BNP (this study) my a
Humbe (Bocage 1893);
L,P BNP (this study) ae
Capelongo (Bogert
L,V 1940); BNP (this study) si a B
P,RR ~~ Handa Farm (this study) A
Humbe (Bocage 1895);
L,V BNP (Butler et al. 2019; Y A,B
this study)
L Osi (= Osse) (Monard B
1937b); Broadley (1981)
Osi (= Osse) (Monard
La 1937b); BNP (Butler et ¥ A,B
al. 2019; this study)
ie Mupa (Monard 1937b) B
L.O Capelongo (Monard AB
1937b); BNP (this study) i
Comment: Scalation features of the specimen (dorsal
head shield with blind lateral sutures (Fig. 14), four
postgenials in the first row, more than seven postgenials
in the second row, two precloacal pores, 204 body
annuli, and 10 caudal annuli) match the description of
M. infuscata (Broadley 1997). In Angola, the species
was recorded in Humbe in Cunene Province, Tombole
River in Cuando-Cubango Province, and a locality
named “Sturuba” (Broadley 1997) which could not be
determined. This is the third confirmed locality for the
Species in the country and the first for Huila Province,
and additional voucher specimens and genetic material
should be collected. Found among sandy soils in Baikea/
Burkea woodlands, Monopeltis anchietae and M.
infuscata are known to be sympatric in Humbe (Broadley
1997), approximately 110 km south of BNP, supporting
their co-occurrence in Carmira Farm.
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
t
yal
Fig. 12. Acanthocercus sp., BNP (male). |
Zygaspis quadrifrons (Peters, 1862)
Kalahari Round-snouted Worm Lizard (Fig. 15)
Material: One unlabelled and bleached specimen in
Carmira Farm’s private collection.
Comment: This specimen conforms morphologically
to Z. quadrifrons (Broadley and Broadley 1997). For
many years, the species was known from Angola only
from Monard’s (1931) description of Amphisbaena
ambuellensis from ‘Chimporo’ (= Tchimpolo), which
was subsequently synonymized with A. qguadrifrons by
Loveridge (1941) and later transferred to Zygaspis by
Alexander and Gans (1966). No additional Angolan
material was collected until recent surveys in southeastern
Angola (Conradie et al. 2016) and BNP (Butler et
ms
x} :
i
> ~
A gees. ea
sft Py ar ita i ae > eS eae
Fig. 13. Monopeltis cf. anchietae, Carmira Farm (Photo by L.
Gata).
Amphib. Reptile Conserv.
al. 2019). Broadley and Broadley (1997) recognized
five groups within Z. qguadrifrons. Additional voucher
specimens and genetic material are necessary to confirm
species identification, and to evaluate the validity of
Monard’s taxon “ambuellensis” for Angolan material
(Branch et al. 2019c). Found in the same habitat as M.
infuscata.
Chamaeleonidae
Chamaeleo dilepis quilensis (Bocage, 1886)
Quilo Flap-necked Chameleon (Fig. 16)
Material: NB760 (33); NB 1084 (C1).
Comment: This subspecies is common and widespread
throughout Angola (Marques et al. 2018). It was recently
recorded in BNP (Butler et al. 2019) and observed
throughout the park, and it has been historically recorded
near BNP (Monard 1937b; Haacke, TM).
Gekkonidae
Chondrodactylus aff. laevigatus (Fischer, 1888)
Button-scaled Gecko
Comment: <A_ large individual of the genus
Chondrodactylus was observed on _ buildings at
Carmira Farm (N. Baptista, pers. obs.), but 1t was not
photographed or collected, and is provisionally assigned
to C. laevigatus based on recent records of this species
from BNP (Butler et al. 2019). Records from near the
park in Mulondo (Schmidt 1933, as Pachydactylus
stellatus), and Humbe (Monard 1937b, as P. bibroni) are
also assigned to this taxon, which is known to occur in
southwestern Angola (Marques et al. 2018).
Lygodactylus angolensis Bocage, 1896
Angola Dwarf Day Gecko (Fig. 17)
Material: NB517 (31).
Comment: Specimens of this taxon were first described
as L. capensis by Bocage (1895), who subsequently
assigned them to a new species, L. angolensis, described
Fig. 14. Monopeltis infuscata, Carmira Farm.
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Fig. 15. Zygaspis quadrifrons, Carmira Farm.
from Hanha, Benguela Province (Bocage 1897). Schmidt
(1933) described a new species of dwarf day gecko, L.
laurae, which was later synonymized with L. angolensis
(Marques et al. 2018; Branch et al. 2019c). Widely
distributed through Africa, localities in Angola were
compiled by Marques et al. (2018) and include Chimboa
da Hanha (= Capira); Cacondo (= Caconda), 2 km W
of; Cubal; Cutenda, 3 km S of; Negola, 6 km S of; and
Quimbango (Haacke, TM). The single BNP specimen
conforms to the original description of L. angolensis
in scalation and coloration, and is similar to specimens
collected in the urban environments of Lubango
(Baptista, unpub. data). Specimens collected at the same
localities (BNP and Lubango) on other occasions have
been assigned to L. bradfieldi (Butler et al. 2019), and
these observations deserve further morphological and
genetic comparisons.
Pachydactylus punctatus Peters, 1854 complex
Speckled Thick-toed Gecko (Fig. 18)
Material: NB513 (14); NB514 (T1); NBS15 (11);
NBS530 (T3); NB773 (34); NB774 (34); NB775 (34).
Comment: This species was recorded in southwestern
Angola (Monard 1937b; Laurent 1964; Marques et al.
2018), including Kului, near BNP (in Monard 1937b
as P. serval, assigned to P. punctatus by Bauer et al.
2006). BNP specimens are morphologically different
ae. ell
Fig. 17. Lygodactylus angolensis, BNP.
Amphib. Reptile Conserv.
Fig. 16. Chamaeleo dilepis quilensis, BNP.
(larger, sturdier, paler, and with a different blotching
pattern) from other specimens found in Tundavala and
Lubango, Huila Province (Baptista et al. 2018; Butler
et al. 2019), that are also assigned to the P punctatus
complex. These lizards also inhabit different habitats
and microhabitats (found on the ground in rocky areas
in Tundavala; under the bark of fallen logs in recently
burnt areas during the day and in leaf litter near a dirt
road during the night in BNP) and very likely belong to
different species. Tundavala is along the high altitude
edge of the Angolan plateau (above 2,000 m asl) and,
given the very specious nature of this genus (Heinicke et
al. 2017) and the existence of cryptic diversity reported
in Angola (Branch et al. 2017), the taxonomic status of
this complex requires further investigation.
Gerrhosauridae
Gerrhosaurus bulsi-multilineatus complex
Plated Lizard (Fig. 19)
Material: NB531 (31); NB776 (2); NB777 (3).
Comment: Five species of Gerrhosaurus are known to
exist in Angola: G. auritus, G. bulsi, G. multilineatus,
G. nigrolineatus, and G. skoogi (Branch et al. 2019c).
Gerrhosaurus nigrolineatus is recorded in areas adjacent
to BNP, in Capelongo and Mulondo (Monard 1937b),
and from the surroundings of Cahama (Haacke, TM).
a on ss ee ‘ .
/ is sh he
a ee Ss, ‘7 Teg .
ee ae r a
Fig. 18. Pachydactylus punctatus complex, BNP.
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 19. Gerrhosaurus bulsi-multilineatus complex (juvenile),
BNP.
Bates et al. (2013) discussed the problematic status of
Angolan populations referred to as G. nigrolineatus,
and species boundaries within the G. bu/si-multilineatus
complex remain unresolved. Assignment of recently
collected specimens is pending until genetic assessment
of the Angolan material is published (M. Bates, pers.
comm.). Specimens collected recently in BNP by Butler
et al. (2019) were assigned to G. cf. multilineatus. One
juvenile was collected in the Main Camp (Fig. 19),
and adults were collected from burrows in degraded
shrubland near the park boundary, and they are similar to
the specimen illustrated in Butler et al. (2019).
Lacertidae
Ichnotropis capensis (Smith, 1838)
Cape Rough-scaled Lizard (Fig. 20A—B)
Material: NB771 (34); NB772 (34); NB779 (12);
photographic record (M. Finckh, site 43).
Comment: /chnotropis capensis and I. bivittata are
known to occur sympatrically in Angola (Laurent 1964;
Marques et al. 2018), and five taxa within this genus
are listed for Angola (Marques et al. 2018; Branch et
al. 2019c). The systematics of the genus /chnotropis is
poorly established (Laurent 1964), and while there is
no recent systematic revision of the group (Edwards et
al. 2013), a thorough historical revision was recently
published (Berg 2017). According to this, two subspecies
of 7. capensis occur in Angola, 1. c. capensis (Smith,
1838) and /. c. overlaeti Witte and Laurent, 1942, with
the latter being restricted to northern Angola (Marques
et al. 2018). Rough-scaled lizards have recently been
collected in BNP and were referred to IJchnotropis
bivittata pallida Laurent, 1964 (Butler et al. 2019), but
we have regarded them as /. capensis, given that J. b.
pallida is morphologically distinct, and occurs in higher
altitudes, such as Humpata (Laurent 1964). Specimens
from BNP have a bright orange/red lateral line that is more
evident in males than in females, and living males have a
bright yellow chin and chest (Fig. 20A—B) that becomes
bleached when preserved. Detailed and comprehensive
studies of species within this genus in Angola are needed.
Amphib. Reptile Conserv.
ota bee at
Fig. 20. Ichnotropis capensis, BNP. (A) Female; (B) male.
Scincidae
Mochlus sundevalli (Smith, 1849)
Sundevall's Writhing Skink (Fig. 21)
Material: One unlabelled bleached specimen in Carmira
Farm’s private collection.
Comment: Widespread throughout eastern and southern
Africa, in Angola this species is recorded from the
coastal plains south of Cuanza River, lower Cuando
River basin (records compiled in Marques et al. [2018]),
and northeastern Angola in Dundo (Laurent 1964).
Panaspis wahlbergi-maculicollis complex
Snake-eyed Skink (Fig. 22A—B)
Material: NB516 (T3); NB548 (T1); NB549 (T2).
Comment: Small leaf-litter inhabiting skinks have nu-
merous cryptic lineages in southern and eastern Africa
(Medina et al. 2016). Historically, Bocage (1895) report-
ed on material from Caconda and Cahata collected by
Anchieta, and recently P. maculicollis was recorded from
southeastern Angola (Conradie et al. 2016). A popula-
tion of “P. wahlberg7” in northern Namibia was shown to
form part of the P. maculicollis complex (Medina et al.
2016) and was subsequently described as a new species,
Panaspis namibiana (Ceriaco et al. 2018a). Snake-eyed
skinks recently collected in BNP were assigned to P. aff.
namibiana (Butler et al. 2019). BNP specimens from this
study have fused anterior parietals, conforming to the P.
wahlbergi complex, but prefrontals are well separated
(see Fig. 22B), distinguishing them from P. namibiana
(Ceriaco et al. 2018a). The taxonomic status of the BNP
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Fig. 21. Mochlus sundevalli, Carmira Farm.
population and its affinities to the P. maculicollis or P.
wahilbergi radiations requires further study, as do other
Angolan populations from Humpata, Quilengues, and the
Cuanza Sul escarpment (Vaz Pinto and Baptista, unpub.
data).
Trachylepis spilogaster (Peters, 1882)
Kalahari Tree Skink
Material: NB519 (31); NB527 (10); NB528 (9); NB529
(13); NB532 (6); NB533 (9); NB778 (31).
Comment: Recently recorded in BNP (Butler et al.
2019), it was the most frequently observed reptile species
during the BNP surveys, and together with Pachydactylus
puntactus, was one of only two species to be found in the
park’s woodlands after recent fires.
Varanidae
Varanus albigularis angolensis Schmidt, 1933
Angolan Savanna Monitor (Fig. 23)
Material: One photographic record (M. Finckh, site 40).
Comment: Several records of Varanus albigularis from
Angola have been assigned to two different subspecies
(Marques et al. 2018). Schmidt (1933) described V. a.
angolensis from *“Gauca, Bihe’ (= Zauca River, Malanje)
(Crawford-Cabral and Mesquitela 1989), and the BNP
record is assigned to this taxon. This species still needs
a wide-ranging phylogenetic assessment. The individual
was observed in the ecotone between grassland and
woodlands.
Serpentes
Colubridae
Crotaphopeltis hotamboeia (Laurenti, 1768)
White-lipped Herald Snake
Material: NB522 (41); four unlabelled specimens in
Carmira Farm’s private collection; one photographic
record from Handa Farm (J. Traguedo, HF).
Comment: A widespread and common species in Angola
(Marques et al. 2018), found active at night, on the edge
of Lagoa Nougalafa (= Nugarrafa, = Nongalafa).
Amphib. Reptile Conserv.
B
+ qs Oe"
—— = 7 pia atk. | :
Rae i
Sod, fm. © si.
fa" We elGt>-s
ie, et Mt oy"
af i ee ie i ope e
e <
ee 7
Fig. 22. Panaspis wahlbergi-maculicollis complex, BNP. Head
(A) lateral view and (B) dorsal view.
Dispholidus typus viridis (Smith, 1838)
Green Boomslang (Fig. 24)
Material: Two unlabelled bleached juvenile specimens
in Carmira Farm’s private collection; one photographic
record (L. Gata, CF).
Comment: Branch (2018) provides an overview of the
two subspecies of boomslang existing in Angola, D. t¢.
punctatus and D. t. viridis. These were shown to deserve
full species status (Eimermacher 2012), but this taxonomic
adjustment requires further consensus. Neither scalation
nor juvenile coloration allow assignment of the Carmira
Farm specimens to either taxon, but the green coloration
of a photographed adult (Fig. 24) is consistent with D. t.
viridis (Eimermacher 2012), as are other material from
Humbe. Resolution of species boundaries in Dispholidus
and the assignment of Angolan populations requires
further genetic studies.
Philothamnus semivariegatus (Smith, 1840) sensu lato
Spotted Bush Snake (Fig. 25)
Material: Two unlabelled bleached specimens in
Carmira Farm’s private collection; one photographic
record from Handa Farm (J. Traguedo, HF).
Comment: The complex taxonomic history of this
Species 1s discussed by Branch (2018). We cautiously
assign specimens from Carmira Farm to P. semivariegatus
based on scalation (three supra-labials entering orbit,
temporal arrangement 2+2, and keeled ventrals),
however, coloration of specimens from both farms did
not have any markings (atypical of P. semivariegatus).
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 23. Varanus albigularis angolensis, BNP (Photo by M.
Finkch).
Historical records from Angola were compiled (Marques
et al. 2018), and additional records include coastal
lowlands in Benguela Province (Vaz Pinto, unpub. data).
This species is paraphyletic having at least four different
lineages (Engelbrecht et al. 2019), and the Carmira
Farm specimens might group with clade 4. Records of
P. angolensis from Capelongo (Bogert 1940) and Humbe
(Haacke, TM) deserve careful comparison with this
material.
Thelotornis capensis oatesi (Gunther, 1881)
Oates' Vine Snake (Fig. 26)
Material: NB1065 (5).
Comment: Widely distributed in Angola, with records
from Hanha (Bogert 1940), Chitado (Hellmich 1957),
Alto Chicapa (Laurent 1964), and Longa (Conradie et
al. 2016). The specimen collected in BNP conforms in
coloration and scalation to this subspecies (see Fig. 26).
Elapidae
Dendroaspis polylepis Gunther, 1864
Black Mamba
Material: Shed skin found in BNP. Photographic records
(L. Gata, CF; J. Traguedo, HF).
Comment: This species is recorded from several
Fig, 24, Disaholidus Apis viridis, Carmira aan (Photo by 2
Gata).
localities in Angola (Marques et al. 2018). Locally
known as “kuiva” (J. Traguedo, pers. comm. ).
Naja anchietae Bocage, 1879
Anchieta's Cobra (Fig. 27A—B)
Material: NB793 (21); NB250 (banded morph) [HF].
Comment: Branch (2018) discusses the description,
history, and taxonomy of N. anchietae in Angola. This
is acommon species occurring in southern Angola, with
known records compiled by Broadley (1995). Recent
records are from Malanje Province (Ceriaco et al. 2014,
Vaz Pinto, unpub. data), on the edge of the plateau in
Tundavala (Baptista et al. 2018), Cassinga (Vaz Pinto,
unpub. data), and Bimbe (Baptista and Vaz Pinto, unpub.
data).
Naja nigricollis Reinhardt, 1843
Black-necked Spitting Cobra (Fig. 28)
Material: Photographic record (J. Traguedo, HF).
Comment: The taxonomy of African cobras (Naja) has
undergone significant changes in recent years (Branch
2018). The name Naja nigricollis has a complex
history of synonymies and varieties, and only when two
varieties, N. n. nigricincta and N. n. woodi, were elevated
to full species, was the name N. nigricollis stabilized to
represent a species (Wuster et al. 2007). It is widespread
Fig. 25. Philothamnus semivariegatus sensu latu, Carmira
Farm.
Amphib. Reptile Conserv.
Fig. 26. Thelotornis capensis oatesi, BNP (Photo by T: ion
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
be
|
Fig. Ep Naja anchietae. (A) BNP (Photo by F- Maiato); (B)
Handa Farm (Photo by J. Traguedo).
in Angola, but avoids dense forest. Locally known as
“turula n'jila” (J. Traguedo, pers. comm. ).
Lamprophiidae
Amblyodipsas ventrimaculata (Roux, 1907)
Kalahari Purple-glossed Snake
Material: NB595 (20); one individual seen in grasslands
near lake from Main Camp (site T3), not collected.
Comment: The specimen’s scalation (15 midbody scale
rows, 21 subcaudals, 203 ventrals, five upperlabials,
2™ and 3™ entering the eye) and coloration (similar to
specimen illustrated in Butler et al. [2019]) conform to
A. ventrimaculata (Branch 1998; Marais 2004). Together
with Butler et al. (2019), BNP is the second record of this
species for Angola, the first being from the Cuito River
source (Portillo et al. 2018; Branch et al. 2019c), and
represents a northwestern extension of the known range
(Botswana, Zimbabwe, Namibia, and Zambia).
Boaedon angolensis (Bocage, 1895)
Angolan House Snake (Fig. 29A—B)
Material: One unlabelled bleached specimen in the
private collection of Carmira Farm.
Comment: This species was recently recorded from BNP
(Butler et al. 2019). The scalation of the Carmira Farm
specimen (23 midbody scale rows, 116 ventrals, more than
55 subcaudals, see Fig. 29A—B for head scalation), accords
with the revision of Angolan house snakes currently in
progress (Hallermann et al., unpub. data).
Amphib. Reptile Conserv.
Ba eae EZ eS ba" eee
igricollis, Handa Farm (Photo by J. Traguedo).
Prosymna angolensis Boulenger, 1915
Angolan Shovel-snout Snake (Fig. 30)
Material: NB521 (T1).
Comment: Originally described from Huila, Angola
(discussion on type locality in Branch [2018]), this
species was recorded historically from southwestern and
central Angola (Marques et al. 2018), and more recently,
from the southeast of Angola (Conradie et al. 2017) and
Tundavala (Baptista, unpub. data). Its upper and lower
labials, ventral scales (145), and low subcaudal counts
(16) conform to the species characterization (Bocage
1895, as P. frontalis). It has gray coloration with a dark
blotch behind the head, a series of paired dark spots
along the back, and immaculate white/creamish belly and
flanks. It was found in sandy soils in miombo woodlands.
Psammophis mossambicus Peters, 1882
Olive Grass Snake (Fig. 31)
Material: NB 518 (head only) (T1); photographic record
(J. Traguedo, HF).
Comment: This species belongs to the P_ sibilans
complex (Kelly et al. 2008, Trape et al. 2019). The
collected snake had a uniformly pale-yellow belly,
and dorsal coloration was plain gray with a thin darker
vertebral dash. Head scalation and ventral (159) and
subcaudal (80) scale counts recorded from the specimen
conform to P. mossambicus (Broadley 2002, Trape et
al. 2019). It is locally known as “muiha on njolo” (J.
Traguedo, pers. comm. ).
Psammophis subtaeniatus Peters, 1882
Stripe-bellied Sand Snake (Fig. 32)
Material: Four unlabelled specimens from Carmira
Farm private collection; one photographic record (L.
Gata, CF).
Comment: This species is restricted to the semi-arid
scrubland and mopane woodland, above and below the
escarpment in southwestern Angola (Branch 2018).
Additional recent records include specimens from
Equimina and Serra da Neve (Vaz Pinto and Baptista,
unpub. data).
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 29. Boaedon angolensis, Carmira Farm. Head (A) lateral
view and (B) dorsal view.
Pseudaspis cana (Linnaeus, 1758)
Mole Snake
Material: One unlabelled specimen from Carmira Farm
private collection; one photographic record (L. Gata,
CF).
Comment: This snake is known from several localities
in Angola (Branch 2018; Marques et al. 2018) and was
recently found in BNP (Butler et al. 2019).
Xenocalamus bicolor bicolor Gunther, 1868
Slender Quill-snouted Snake (Fig. 33A—B)
Material: Two unlabelled specimens in the private
collection of Carmira Farm.
Comment: Xenocalamus bicolor is only recorded in
Angola from a northern subspecies described in the
northeast of the country, X. b. machadoi (see Broadley
1971; Branch 2018; Marques et al. 2018). It occurs in
the Zambezi Region and adjacent western Zambia, and
it is usually associated with Kalahari sands (Branch et
Fig. 31. Psammophis mossambicus, Handa Farm (Photo by J.
Traguedo).
Amphib. Reptile Conserv.
Fig. 30. Prosymna angolensis, BNP.
al. 2019). Its presence was considered to be likely for
southeastern Angola (Branch et al. 2019), and this record
is the first for the country. The presence of supraoculars
separating the frontals from contacting the orbit (Fig.
33B), conforms to _X. b. bicolor, as does the number of
ventrals (204, 233) [Broadley 1971]. Xenocalamus b.
bicolor is known to have great intraspecific variation in
coloration, and this feature is rarely diagnostic (Broadley
1971). The patterns of both Carmira Farm specimens
resemble the “maculatus” phase described by Broadley
(1971), but more heavily marked (Fig. 33A).
Leptotyphlopidae
Namibiana aff. rostrata (Bocage, 1886)
Angolan Beaked Thread Snake (Fig. 34)
Material: NB599 (HF).
Comment: Thread snakes are a difficult group to study
due to their very small size and conservative morphology
(Broadley and Broadley 1999; Branch 2018). Namibiana
rostrata is endemic to Angola, and originally described
from Humbe, ca. 110 km south of BNP. It has recently
been recorded from BNP (Butler et al. 2019), and we
provisionally assign the specimen from Handa Farm to the
same species. Haacke (TM) collected two thread snakes,
one from Paiva Couceiro (= Quipungo, TM45190),
around 30 km southeast of Handa Farm, and another
from Hoque (TM 46699), ca. 77 km northwest of BNP,
~~
Fig. 32. Psammophis subtaeniatus, Carmira Farm.
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
Fig. 33. Xenocalamus bicolor bicolor, Carmira Farm. (A) Full
specimen; (B) dorsal view of head.
both identified as Leptotyohlops scutifrons scutifrons. All
these records should be carefully compared to confirm
species identification.
Pythonidae
Python anchietae Bocage, 1877
Namib Dwarf Python
Comment: Python anchietae is endemic to the Namib
Desert and adjacent areas in Angola and Namibia. It was
collected in Viriambundo (Haacke, TM), ca. 30 km west
of BNP. Although this is a historical record, it is discussed
in the species accounts here due to its relevance. This is
the fourth known record of this near-endemic species in
the country, after the type locality Catumbela (Bocage
1887), Hanha (Bogert 1940), and between Lobito and
Hanha (Laurent 1964), and the first record above the
Angolan escarpment. In Namibia, it occurs inland up to
near Windhoek, indicating that the species may extend
further inland in Angola and occur in BNP.
Amphib. Reptile Conserv.
Fig. 35. Afrotyphlops cf. schlegelii, BNP (Photo by M. Finkch).
Python natalensis Smith, 1840
Southern African Python
Material: NB794 (1); one individual observed in BNP’s
hide for game viewing (27); one photographic record
from Carmira Farm (L. Gata, CF); several photographic
records from Handa Farm (J. Traguedo, HF).
Comment: Two species of African python exist in
Angola, the northern P sebae, and the southern P
natalensis (Branch 2018). Material from BNP belongs to
P. natalensis.
Typhlopidae
Afrotyphlops cf. schlegelii (Bianconi, 1849)
Schlegel's Blind Snake (Fig. 35)
Material: Photographic record (M. Finckh, 39).
Comment: One specimen was photographed after heavy
rainfall at night (nearly 100 mm of precipitation). Dorsal
coloration was dark yellowish with scattered dark blotches
(Fig. 35) and snout-vent length measured around 70 cm
(M. Finckh, pers. comm.). Afrotyphlops schlegelii is a
sister species of A. mucruso, and both have been recorded
from Angola. Marques et al. (2018) limit A. mucruso to
northeastern Angola, and A. schlegelii to the southwest,
and Haacke (TM) also has records for Huila Province
(as Rhinotyphlops schlegelii petersii). A taxonomic
discussion is presented in Broadley and Wallach (2009),
and further discussions of both species in Angola are
presented by Conradie et al. (2016) and Branch (2018).
Confident identification requires additional material, and
the genus deserves further taxonomic revisions.
Viperidae
Bitis arietans Merrem, 1820
Puff Adder
Material: NB713 (19); one photographic record and one
specimen from Carmira Farm private collection.
Comment: Common and widespread in Angola,
recorded from several localities (Bocage 1895; Ferreira
1897; Schmidt 1933; Bogert 1940; Hellmich 1957;
Laurent 1950, 1954, 1964: Thys van der Audenaerde
1967; Manacgas 1981; Conradie et al. 2016), with few
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Fig. 36. Causus rhombeatus, Handa Farm (Photo by J.
Traguedo).
records from the southwest (Branch 2018; Marques et al.
2018). In Angola, it is widely known as “surucucu.”
Causus rhombeatus (Lichtenstein, 1923)
Rhombic Night Adder (Fig. 36)
Material: Photographic record from Handa Farm (J.
Traguedo, HF).
Comment: The taxonomy of night adders in Angola has
long been confusing (Branch 2018). Causus bilineatus was
described from a variety of C. rhombeatus by Boulenger
(1905), but synonymies and species validity remained
problematic until a recent revision by Rasmussen
(2005), who reassessed C. bilineatus and related species,
mapped the geographic distribution of Angolan night
adders, and provided a key to the genus. Scale counts
could not be made on the specimen from Handa Farm,
although the photographed snake had a very conspicuous
V-shaped marking on the head, 25 well-separated dark
conspicuous rhombic vertebral markings occasionally
with a white contour against a paler background, and
lacked dorsolateral stripes (Fig. 36). It was therefore
assigned to C. rhombeatus, which is widespread in Angola
(Rasmussen 2005; Marques et al. 2018).
Testudines
Pelomedusidae
Pelomedusa subrufa (Bonnaterre, 1789)
Marsh Terrapin
Material: NB780 (35); photographic record (M. Finckh,
site 43).
Comment: This species is widespread in southern,
eastern, and western Africa (Branch 2012; Turtle
Taxonomy Working Group 2017). It has been recorded
from several localities in Angola (Marques et al. 2018),
and recently from BNP (Butler et al. 2019). Petzold et
al. (2014) recorded unexpected species diversity in
Amphib. Reptile Conserv.
a molecular phylogeny of Pelomedusa and referred
northern Namibian material to P. subrufa.
Testudinidae
Kinixys cf. belliana Gray, 1831
Bell’s Hingeback Tortoise
Material: NB711 (18); NB712 (17); NB509 (16) (tissue
only); photographic record (M. Finckh, site 43).
Comment: In a molecular phylogeny of Kinixys, only
K. belliana was shown to occur in Angola (Kindler et
al. 2012). However, only northern Angolan material was
included and it is very likely that K. spekii may enter
southern Angola (see Marques et al. 2018), thus the
identification as K. belliana 1s tentative. This group is
widely distributed in Angola (Marques et al. 2018) and
has recently been collected in BNP (Butler et al. 2019).
This species has been observed at several sites throughout
the park and 1s locally harvested for consumption and for
the pet trade.
Crocodilia
Crocodilydae
Crocodylus niloticus Laurenti, 1768
Nile Crocodile
Material: Interviews.
Comment: Staff from BNP referred to the existence of
this species in the Cunene River, the eastern boundary of
the park. Historical records mention its occurrence in the
area (Monard 1937b; Sim6es 1971).
Discussion
This account presents one new record for the country
(Xenocalamus bicolor bicolor), as well as records
of reptile species that are potentially new to science
(Pachydactylus, Namibiana). Butler et al. (2019)
reported eight amphibian taxa and 21 reptile taxa (two
testudines, 14 lizards, and five snakes) from BNP and
adjacent Capelongo, while this study doubles the number
of amphibian species (16), and almost quadruples
the number of snake species (18) encountered. These
increases in known species diversity are more significant
when compared to the total species counts (94, including
historical records) for the region. Despite the considerable
udpate in knowledge that this study presents, further
surveys are likely to describe additional diversity.
Closely related taxa recorded in this study and by Butler
et al. (2019), namely Lygodactylus angolensis and L.
bradfieldi, require further research and comprehensive
comparisons to confirm whether they refer to sympatric
congeneric species or different designations of the same
taxa.
Ambiguous taxonomy reflects the unresolved status
of Angolan herpetology, as the bulk of species accounts
December 2019 | Volume 13 | Number 2 | e203
Herpetofauna of Bicuar National Park, Angola
presented here refer to problematic taxonomy and a
lack of supporting studies. This is true even for the BNP
region, which is situated within the southwest, the more
thoroughly studied part of the country. This knowledge
gap reinforces the importance of promoting surveys
which include voucher specimens and DNA sample
collections published with survey results, as highlighted
previously (Russo et al. 2019). The inclusion of DNA
barcoding for identification purposes is increasingly
common (Bittencourt-Silva 2019) and provides a more
comprehensive understanding of the results. Although
not included in the scope of this publication, biopsies and
specimens collected are being used for ongoing studies
(Baptista et al., unpub. data; Lobon-Rovira et al., unpub.
data).
The herpetofauna of the BNP region is similar to that
of other regions further east where Kalahari sands are
also the dominant substrate. It shares 12 amphibian and
30 reptilian species with southeastern Angola (Conradie
et al. 2016); seven amphibian and 20 reptilian species
with western Zambia, Ngoye Falls, and surrounding
areas (Pietersen et al. 2017); and nine amphibian and five
reptilian species with recently surveyed areas of west
Zambia (Bittencourt-Silva 2019).
In a study of herpetofauna in the southern Kalahari
domain, Haacke (1984) noted the relevance ofa latitudinal
rainfall gradient as a driver of diversity in the Kalahari.
This gradient affects vegetation canopy structure on a
wide scale in Botswana (Scholes et al. 2004), and it is also
reflected in the avifauna species assemblages of BNP,
which comprise biome-restricted species from both the
northern Angolan Miombo Woodland and the southern
Zambezian Baikiaea Woodland ecoregions (Dean 2000;
BirdLife International 2018). The effect of this gradient
on the herpetofauna of BNP is not yet known, and would
be an interesting research topic for understanding the
relevance of BNP for conserving herpetofauna. Records
of species that were previously only reported from
the coastal plain of Angola, such as Python anchietae,
have shown that they occur above the escarpment. This
shows how studying the park’s herpetofauna may also
contribute to understanding the west-to-east altitudinal
and rainfall gradients, and the distribution limits of
plateau and lowland species.
Monopeltis perplexus, an endemic Angolan
amphisbaenian, was originally described from a vague
type locality: “Hanha or Capelongo” (see discussion in
Branch et al. 2018). If Capelongo (9 km northeast of
BNP) is confirmed as the type locality, M. perplexus is
likely to occur in BNP and would be sympatric with M
anchietae and M. infuscata. Sympatric distributions of
amphisbaenians highlight the importance of Kalahari
sands for fossorial species. Although fossorial species
are well represented in the BNP region, the absence
of fossorial groups such as Acontias, Typhlacontias,
and Sepsina, which have been recorded from adjacent
areas on Kalahari sands (Monard 1937b; Branch and
Amphib. Reptile Conserv.
McCartney 1992; Haacke 1997; Conradie et al. 2016;
Pietersen et al. 2017; Marques et al. 2018; Bittencourt-
Silva 2019) is likely a result of undersampling.
Rupicolous species such as Cordylus machadoi,
Matobosaurus maltzahni, Hemirhagerrhis viperina,
and Agama p. schaki were not found in the park despite
historical records, likely as a reflection of the rarity of
rocky outcrops. Substrate specificity and isolation have
important influences on the geographic distribution of
reptiles, especially lizards, and are considered better
determinants of presence than vegetation type (Bauer
and Lamb 2005; Roll et al. 2017). Endemic sand-adapted
reptiles were reported in the Kalahari (Haacke 1984).
The BNP region has a small contact zone with the larger
Kalahari sands block to the east (Missao de Pedologia
de Angola 1959; Huntley 2019). Moreover, the park is
delimited in the east by the large Cunene River, which
may be a barrier to species dispersal, much like the
Zambezi River (Pietersen et al. 2017). The combination
of factors driving speciation in the BNP region, especially
for fossorial species, is thus still unclear, and may be
clarified by assessing the genetic divergence between
BNP specimens and those from the easternmost regions
of the Kalahari sands (e.g., southeastern Angola).
Commercial and small-scale farms occupy large
portions of northwest BNP (Mendelsohn and Mendelsohn
2018). Additional disturbances include poaching and
conversion of woodlands into thickets and shrubland
following intense and frequent fires (Mendelsohn
and Mendelsohn 2018; Mendelsohn 2019). Several
mammalian species are either extinct or on the verge of
extinction in the park (Overton et al. 2017; Mendelsohn
and Mendelsohn 2018), but the consequences of these
disturbances for herpetofauna are largely unknown. Some
species are reportedly collected opportunistically for the
pet and bushmeat trades (e.g., Kinixys), a phenomenon
that has also occurred in Cangandala National Park
(Ceriaco et al. 2018c).
The establishment of protected areas generally favors
the conservation of mammals, birds, and amphibians,
while reptiles are usually neglected (Roll et al. 2017).
Likewise, the distributions of large mammals in Angola
has defined the designation of conservation areas (Huntley
et al. 2019a). BNP is an Important Bird and Biodiversity
Area, relevant for the conservation of avifauna (Dean
2000; BirdLife International 2018) that also supports
considerable reptile diversity. Some of the species likely
to occur in the park are endemic to Angola (Monopeltis
perplexus, Nucras broadleyi, Psammophylax ocellatus,
Namibiana rostrata), to Angola and Namibia (Python
anchietae), or are poorly studied (Mertensophryne
mocquardi). A better understanding of the park’s
herpetofauna should reinforce its important role in the
conservation of Angolan biodiversity.
Acknowledgements.—This research was carried out
in the framework of the Southern African Science
December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Service Centre for Climate Change and Adaptive Land
Management (SASSCAL) project, sponsored by the
German Federal Ministry of Education and Research
(BMBF) under promotion number 01LG1201M.
Collection of specimens took place under the
Memorandum of Understanding between the Angolan
Ministry of Environment (MINAMB/INBAC) and
ISCED-Huila. This work benefited from logistical and
administrative support, records of species, access to
literature, discussions on the subject, and revisions of
the manuscript. For these we thank (alphabetically):
Adam Marques, Aimy Caceres, Bicuar National Park
(Administrator José Maria Kandungo, park rangers
and staff), Brian J. Huntley, Carmira Farm (Luis Gata,
Ernesto Preto), Governo Provincial da Huila, Handa
Farm (General Joao Traguedo), ISCED-Huila (Fernanda
Lages, Filipe Rocha, Francisco Maiato, José Luis
Alexandre, Manfred Finckh, Milciades Chicomo, Paulina
Zigelski, Valter Chissingui), John Mendelsohn, Luis
Verissimo (who provided BNP boundaries and official
gazetting information), Luke Verburgt, Michael Mills,
Pedro Vaz Pinto, SAo Neto, Sasha Vasconcelos, Sidney
Novoa, and Werner Conradie. Special thanks to Alan
Channing and Wulf Haacke, who provided unpublished
records and permission to use them. NB is currently
supported by FCT contract SFRH/PD/BD/140810/2018.
Bill Branch (1946-2018) passed away during the revision
process of this paper. In the later years of his career,
Bill dedicated considerable time and effort to studying
the Angolan herpetofauna, creating local expertise, and
stimulating surveys and publications, which have led
to remarkable findings and incommensurable advances
in the knowledge of this field. It was a privilege and an
honor for the co-authors to work with Bill on this project.
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Amphib. Reptile Conserv.
Ninda Baptista is anAngolan conservation biologist with ten years of experience inthe environmental
and conservation sectors in Angola. From 2015 to 2018, Ninda worked for the Southern African
Science Service Centre for Climate Change and Adaptive Land Management (SASSCAL) Project
at Instituto Superior de Ciéncias da Educagéo da Huila (ISCED - Huila). There she conducted
herpetological surveys and monitoring, and created a herpetological collection of Angolan
specimens. Her recent experience includes working as an assistant herpetologist in the National
= Geographic/Okavango Wilderness Project, in applied conservation in Angolan scarp forests in a
Conservation Leadership Programme-funded project, and on environmental education. Ninda is an
author of scientific papers and book chapters on Angolan herpetology and ornithology, as well as
magazine articles and books for children about Angolan biodiversity.
Telmo Antonio is an Angolan biologist who recently graduated in Biology Teaching from ISCED-
Huila, with an honors thesis on the grasses of Tundavala. Telmo worked as research intern in the
SASSCAL project at ISCED-Huila from 2016 to 2018, participating in all tasks related to plants,
mammals, and herpetofauna, especially in Tundavala and Bicuar National Park. Telmo taught
high-school Biology in Lubango, Angola. He is currently a Natural Resources Management M.Sc.
student in the Namibia University of Science and Technology, within the SCIONA Project “Co-
designing conservation technologies for Iona - Skeleton Coast Transfrontier Conservation Area
(Angola - Namibia),” which is funded by the European Union.
Bill Branch (1946-2018) was born in London and worked as Curator of Herpetology at the Port
Elizabeth Museum for over 30 years (1979-2011), and upon his retirement he was appointed
as Curator Emeritus of Herpetology. His herpetological studies have focused mainly on the
systematics, phylogenetic relationships, and conservation of African reptiles. He has published
over 300 scientific papers, and numerous popular articles and books. The latter include: South
African Red Data Book of Reptiles and Amphibians (1988), Dangerous Snakes of Africa (1995,
with Steve Spawls), Field Guide to the Reptiles of Southern Africa (1998), Tortoises, Terrapins
and Turtles of Africa (2008), and Atlas and Red Data Book of the Reptiles of South Africa, Lesotho
and Swaziland (multi-authored, 2014), as well as smaller photographic guides. In 2004 Bill was
the 4" recipient of the “Exceptional Contribution to Herpetology” award of the Herpetological
Association of Africa. Bill has undertaken field work in over 16 African countries, and described
nearly 50 species, including geckos, lacertids, chameleons, cordylids, tortoises, adders, and
frogs. He supervised all tasks related to herpetology in the SASSCAL project, the creation of a
herpetofauna archive in ISCED-Huila, and many other ongoing initiatives in Angolan herpetology.
128 December 2019 | Volume 13 | Number 2 | e203
Baptista et al.
Appendix 1. List of collecting sites in Bicuar National Park, Angola, and surroundings, with coordinates (decimal degrees).
Asterisks (*) indicate sites located outside of the park. Sampling method: AS = active searching or opportunistic observation; DOR
= dead on road; T = trapping.
: : . : % ,
Site Name Latitude (°S) Longitude (°E) range tiethod Habitat type
1 BNP, road between -15.610300 14.879561 6 Nov 2017 DOR Grassland along Luconda drainage line
Tunda Gate and Main
Camp
ps BNP, near Tchiwacussi -15.189030 15.254460 6 Nov 2017 AS Secondary growth scrubland in old crop
fields, near Tambi drainage line
3 BNP -15.177040 15.228570 6 Nov 2017 AS Degraded scrubland near Tambi drainage
line
5 BNP -15.148550 14.841380 16 Mar 2018 AS Miombo woodland with considerable
bush encroachment
6 BNP -15.130452 14.683723 6 Dec 2016 AS Recently burnt open miombo woodland
7 BNP -15.129961 14.730298 6 Dec 2016 AS Temporary pond along Bicuar drainage
line
9 BNP -15.126656 14.637726 6 Dec 2016 AS Recently burnt open miombo woodland
10 BNP -15.126032 14.601210 6 Dec 2016 AS Open miombo woodland
12. BNP, road along Bicuar -15.104853 14.840320 7 Nov 2017 AS Grassland
drainage line
13. BNP -15.100510 14.845050 6 Dec 2016 AS Open miombo woodland
14. BNP, close to Main -15.096715 14.839058 2 Dec 2016 AS Leaf litter accumulated along the road, in
Camp, road to Hombo open miombo woodland
gate
15 BNP, drainage line -15.092432 14.836883 2 Dec 2016 AS Grassland
upstream Main Camp
water hole
16 BNP, road between -15.082880 14.928760 2 Dec 2016 AS Dense miombo woodland
Capelongo Gate and
Lagoa da Matemba
17 BNP, road between -15.057374 14.932907 7 Dec 2017 AS Dense miombo woodland
Capelongo Gate and
Main Camp
18 BNP, road between -15.036282 14.959543 7 Dec 2017 AS Mosaic of dense miombo woodland and
Capelongo Gate and shrubland
Main Camp
19 BNP -15.160722 14.859036 7 Dec 2017 AS Miombo woodland
20 BNP -15.129161 14.881776 2 Jul 2017 AS Open miombo woodland
21* Outskirts of BNP -14.945094 15.095214 6 Nov 2017 DOR Degraded open shrubland
25 Lagoa da Matemba -15.122320 14.902980 4 Nov 2017 AS Permanent water body with aquatic
vegetation
26 Lagoa do Dyjimbi -15.145520 14.914670 5 Nov 2017 AS Permanent water body
27 Main Camp water whole -15.102406 14.836857 8 Dec 2016 AS Permanent water body
28 Main Camp water whole -15.098320 14.837030 7 Dec 2016 AS Permanent water body
29 Main Camp water whole -15.098060 14.836990 7 Dec 2016 AS Permanent water body
30 ‘Drainage line upstream -15.093490 14.837450 4 Dec 2016 AS Grassland
Main Camp water whole
31 BNP Main Camp -15.100725 14.839557 2009-2017 AS Human facilities, sandy soils, tall Burkea
africana trees, surrounded miombo
woodland
32* Outskirts of BNP -15.060080 15.251800 6 Nov 2017 AS Degraded open shrubland
33. BNP -15.150060 14.812300 5 Nov 2017 AS Miombo woodland with considerable
bush encroachment
34 BNP, near Bicuar drain- -15.243460 14.891460 5 Nov 2017 AS Recently burnt open miombo woodland
age line
35 BNP, road between -15.024986 14.796841 4 Nov 2017 AS Open miombo woodland with regenerat-
Hombo Gate and Main ing understorey
Camp
Amphib. Reptile Conserv. 129 December 2019 | Volume 13 | Number 2 | e203
Date or date
Sampling
Herpetofauna of Bicuar National Park, Angola
Appendix 1. List of collecting sites in Bicuar National Park, Angola, and surroundings, with coordinates (decimal degrees).
Asterisks (*) indicate sites located outside of the park. Sampling method: AS = active searching or opportunistic observation; DOR
= dead on road; T = trapping.
Date ordate Sampling
‘ ‘ A ‘ 2% ‘
Site Name Latitude (°S) Longitude (°E) ranige method Habitat type
36 ~~ BNP, close to Main -15.095409 14.838751 2 Nov 2016 AS Miombo woodland
Camp, road to Hombo
gate
39 BNP, Tunda Gate -15.645000 14.708333 6 Dec 2015 AS Dry woodland on deep sands
40 BNP -15.133300 14.900000 11 Dec 2015 AS Ecotone between grassland and wood-
land
41* Lagoa Nougalafa, out- -14.977117 14.693638 6 Dec 2016 AS Permanent water body
skirts of BNP
42* Between Chibemba and -16.03 14.20 15 Feb 2010 AS Small wetland, approximate coordinates
Cahama
43. BNP -15.042928 14.805010 5 Dec 2016 AS Border of one a grassland valley, in the
ecotone between suffrutex grasslands
and woodland, crossing sandy dirt road
CF* Carmira Farm -16.044722 14.569167 2015-2018 AS Baikiaea/Burkea woodland, deep Kala-
hari sands
C1* Road to Carmira Farm -15.992383 14.410287 5 Apr 2018 AS Baikiaea/Burkea woodland, deep Kala-
hari sands
HF* Handa Farm -14.699722 14.295833 2015-2018 AS Degraded miombo woodland with over-
grazing and deforestation
ast Woodland trapline 1 -15.094405 14.838312 2-7 Dec T Miombo woodland not burnt for more
2016 than 1 year
T2 Woodland trapline 2 -15.100358 14.838958 7-10 Dec Ak Miombo woodland not burnt for more
2016 than 5 years
T3 Grassland trapline -15.102190 14.837057 2-10 Dec Mt Grassland near permanent body of water
2016
Amphib. Reptile Conserv. 130 December 2019 | Volume 13 | Number 2 | e203
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 1-13 (e183).
First record of the Cat Ba Tiger Gecko, Goniurosaurus
catbaensis, from Ha Long Bay, Quang Ninh Province,
Vietnam: microhabitat selection, potential distribution,
and evidence of threats
19.10Hai Ngoc Ngo, 7Tuan Quang Le, *Minh Le Pham, 2?Truong Quang Nguyen,
56.7Minh Duc Le, Mona van Schingen, and *:"°*Thomas Ziegler
'Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, VIETNAM Institute of
Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, VIETNAM°?Graduate University
of Science and Technology, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, VIETNAM *Ha Long Bay Management
Department, 166 Le Thanh Tong Road, Ha Long, Ha Long City, Quang Ninh, VIETNAM *Faculty of Environmental Sciences, Hanoi University of
Science, Vietnam National University, 334 Nguyen Trai Road, Hanoi, VIETNAM °Central Institute for Natural Resources and Environmental Studies,
Hanoi National University, 19 Le Thanh Tong, Hanoi, VIETNAM ‘Department of Herpetology, American Museum of Natural History, Central Park
West at 79 Street, New York, New York 10024, USA *Federal Agency for Nature Conservation, CITIES Scientific Authority, Konstantinstrasse 110,
53179 Bonn, GERMANY * Institute of Zoology, University of Cologne, Ziilpicher StraBe 47b, 50674, KéIn, GERMANY '°Cologne Zoo, Riehler Strape
173, 50735, KélIn, GERMANY
Abstract.—The Cat Ba Tiger Gecko (Goniurosaurus catbaensis) was described from Cat Ba Island, Hai Phong,
northern Vietnam in 2008, while a presumed congener was recently spotted from another offshore island in
the Ha Long Bay. During the field surveys reported here, new Goniurosaurus occurrences were discovered
for the first time on small offshore islands in the Ha Long Bay, Quang Ninh Province. These were identified
and confirmed as G. catbaensis based on morphological and molecular data. However, these newly found
populations are very small and exposed to increasing anthropogenic pressures. Since knowledge about the
species ecology remains poor, the first microhabitat characterization for G. catbaensis is provided herein, which
is essential for conservation of the species as well as its natural habitats. Sex- and age-related differences in
selection of perch height are herein presented. In addition, we present evidence for various anthropogenic
threats such as regular trade in living tiger geckos (including G. catbaensis) on local markets in Hai Phong and
Ho Chi Minh cities, Vietnam. These findings highlight the need for more stringent conservation measures to
reduce human impacts on the extremely small, insular populations of the Cat Ba Tiger Gecko.
Key words. Anthropogenic pressure, conservation, ecology, offshore islands, phylogram, trade
Citation: Ngo HN, Le TQ, Pham ML, Nguyen TQ, Le MD, van Schingen M, Ziegler T. 2019. First record of the Cat Ba Tiger Gecko, Goniurosaurus
catbaensis, from Ha Long Bay, Quang Ninh Province, Vietnam: microhabitat selection, potential distribution, and evidence of threats. Amphibian &
Reptile Conservation 13(2) [General Section]: 1-13 (e183).
Copyright: © 2019 Ngo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0
International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any me-
dium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as
follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Submitted: 18 July 2017; Accepted: 27 February 2019; Published: 2 September 2019
Introduction araneus, G. catbaensis, G. huuliensis, G. lichtenfelderi,
and G. /uii (Nguyen et al. 2009). Among these species, the
The genus Goniurosaurus currently comprises 19
species with a disjunct distribution in southern East Asia.
Most Goniurosaurus species are endemic with restricted
distribution ranges (Chen et al. 2014; Grismer et al. 1994,
1999; Honda and Ota 2017; Seufer et al. 2005; Yang and
Chan 2015; Zhou et al. 2018; Ziegler et al. 2008). Habitat
degradation and overharvesting for the pet trade were
identified as major threats to wild populations of tiger
geckos (Yang and Chan 2015). At present, five species
of Goniurosaurus are known from Vietnam, namely G.
Correspondence. * ziegler@koelnerzoo.de
Amphib. Reptile Conserv.
insular Cat Ba Tiger Gecko (Goniurosaurus catbaensis)
was discovered on Cat Ba Island in Cat Hai District,
Hai Phong City, northeastern Vietnam, where it was
assumed to be endemic (Ziegler et al. 2008). Preliminary
population assessments of G. catbaensis revealed that its
effective population size, defined as number of mature
individuals, is much smaller than the suggested threshold
values for minimal viable populations to maintain a stable
population in the long term (Ngo et al. 2016; Nguyen
et al. 2016, 2018; Reed et al. 2003; Traill et al. 2007).
September 2019 | Volume 13 | Number 2 | e183
Goniurosaurus catbaensis in Ha Long Bay, Vietnam
i op ae Ae , ; at! t ea rah
Fig. 1. New population. (A) Habitat of Goniurosaurus
be? ee # te a OP EAs)
catbaensis on one offshore island in
+' wide’ ‘ie of : * :
Laer “S ee ae =.
Ro Se ef Po
ae
Ha Long Bay, Quang Ninh Province:
(B) Microhabitat of G. catbaensis in Ha Long Bay; (C) Adult male; and (D) Adult female from Ha Long Bay. Photos: H.N. Ngo.
Even in undisturbed habitats, G. catbaensis occurs at low
densities (Ngo et al. 2016; Nguyen et al. 2016, 2018).
The insular Cat Ba Tiger Gecko was found to be
vulnerable to anthropogenic disturbances, and of high
demand in pet markets as well as on Internet platforms
(Ngo et al. 2016; Nguyen et al. 2018). In addition to
poaching, habitat destruction for touristic purposes
has dramatically increased the pressure on the wild
G. catbaensis population. Consequently, the need for
protection of the Cat Ba Tiger Gecko has received
growing attention. Based on the first international
population and trade investigations, this species has
recently been listed in the IUCN Red List of Threatened
Species as "Endangered" (Nguyen et al. 2016). The
wild population is probably in peril due to its restricted
distribution range, rising anthropogenic threats, and the
lack of appropriate conservation measures. For the latter,
detailed information on habitat requirements and the
exact distribution of this species is essential, but such
data are currently lacking. Ngo et al. (2016) recently
suggested the potential occurrence of G. catbaensis on at
least one more offshore island in Ha Long Bay.
To confirm this possibility, we investigated other small
offshore islands in Ha Long Bay, Quang Ninh Province
to locate populations of G. catbaensis, and predicted the
overall availability of suitable habitats for the species in
northeast Vietnam. In addition, the present study aimed
to provide the first data on microhabitat selection of G.
catbaensis. We assumed that differences in habitat use
would occur between age classes and sexes, as they have
Amphib. Reptile Conserv.
been observed in other lizards (Snyder et al. 2010; van
Schingen et al. 2015).
Materials and Methods
Study areas: Study sites were selected based on our
previous surveys on Cat Ba Island, Hai Phong City,
and on photo documentation which gave evidence for
the possible occurrence of Goniurosaurus on a small
island in Ha Long Bay, Quang Ninh Province (Ngo et
al. 2016). Cat Ba Island and adjacent islands comprise
isolated limestone karst formations, which provide
diverse habitats for a unique flora and fauna (Clements
et al. 2006). Cat Ba Archipelago was recognized as the
“Cat Ba Archipelago Biosphere Reserve” (CBBR) by
the United Nations Educational, Scientific and Cultural
Organization (UNESCO) in 2004 due to its significant
ecosystem and biodiversity values (CBBR Authority
2013). Ha Long Bay was also twice recognized (in 1994
and 2000) by UNESCO as a World Heritage Site for the
outstanding universal value of its landscape, geology, and
geomorphology (The Management Department of Ha
Long Bay 2014). Both areas are among the most popular
tourist destinations in Vietnam, and face challenges from
rapid tourism development.
Field surveys: Field surveys were conducted on Cat
Ba Island between June and August 2014, May 2015,
and during a short time in June 2016, which fell in the
non-hibernation season of Goniurosaurus (Grismer et
September 2019 | Volume 13 | Number 2 | e183
Ngo et al.
al. 1999; Ngo et al. 2016). Furthermore, six offshore
islands in Ha Long Bay, situated in close proximity to
Cat Ba Archipelago, were surveyed in July 2016. Night
excursions were conducted between 7:30 and 11:30
PM, when the lizards were found to be active (Ngo et
al. 2016; Ziegler et al. 2008). To measure morphological
characters, the animals were captured by hand and
subsequently released at the same spot after checking and
taking measurements.
Ecological analyses: Microhabitat data were recorded
for each sighted G. catbaensis, including substrate
types (classified as cliff, rock, branch, sand, or forest
floor), perch height (vertical distance between captured
animal and ground, in cm), percentage of vegetation or
cave coverage, position (resting outside or inside cave),
substrate surface condition (dry or wet), and activity
(resting, feeding, or foraging). Air temperature and
relative humidity were measured with a digital thermo-
hygrometer (TFA Dostmann/Wertheim Kat. Nr. 30.5015),
and substrate temperature and body surface temperature
of animals were measured with an infrared thermometer
(Measupro IRT20).
To identify intraspecific differences in microhabitat
selection by G. catbaensis, individuals were classified
into different age classes according to their snout-vent
lengths (SVL): SVL < 85 mm = juvenile, SVL > 85 mm
and < 105 mm = sub-adult, and SVL => 105 mm = adult
(Ngo et al. 2016). Adults were differentiated between
the sexes, as well as between gravid and non-gravid
individuals. Sex of specimens was determined by the
presence of the large swollen hemipenal bulges in males,
while non-swollen in females.
A t-test, with @ = 0.05, was performed to determine
differences in microhabitat parameters between age
classes and sexes. Statistical analyses were performed
with the program PAST, Version 2.17c (Hammer et al.
2001).
Morphological analyses: Morphometric measurements
of captured individuals were taken with a digital caliper
to the nearest 0.1 mm. In addition, two voucher specimens
of the newly discovered populations in Ha Long Bay were
collected, euthanized with ethylacetate, preserved in 70%
ethanol, and deposited in the collections of the Vietnam
National Museum of Nature (VNMN), Hanoi, Vietnam
(VNMN 05423, VNMN 05424). Morphological characters
were taken according to Ngo et al. (2016), Orlov et al.
(2008), Yang and Chan (2015), and Ziegler et al. (2008).
Abbreviations of measurements are as follows: snout
vent length (SVL) from tip of snout to vent; tail length
(TaL) from vent to tip of tail; distance between axilla
and groin (AG) from posterior edge of forelimb insertion
to anterior edge of hind limb insertion; forelimb length
(FoL) from axilla to tip of longest finger; hindlimb length
(HiL) from groin to tip of longest finger; snout to eye
distance (SE) from tip of snout to anterior-most point of
eye; eye to ear distance (EE) from posterior margin of eye
to posterior margin of ear; orbital diameter (OD) greatest
diameter of orbit; ear diameter (ED) longest dimension
of ear; internarial distance (IND) as distance between
nares; anterior eye distance (AED) as distance between
Amphib. Reptile Conserv.
anterior corners of eyelids; posterior eye distance
(PED) as distance between posterior corners of eyelids;
maximum head width (HW); maximum head height
(HH); head length (HL) from tip of snout to posterior
edge of occiput; pileus length (PL) from tip of snout to
posterior scale of the head; and jaw length (JL).
Abbreviations of scalation are as follows: supralabials
(SPL); infralabials (IFL); nasal scales surrounding
nare (N); internasals (IN); gular scales bordering the
internasals (PostIN); postmentals (PM); gular scales
bordering the postmentals (GP); eyelid fringe scales
or ciliaria (CIL); granular scales surrounding dorsal
tubercles (GST); dorsal tubercle rows at midbody
(DTR); paravertebral tubercles between limb insertions
(TL); scales around midbody (MB); subdigital lamellae
under the first finger (LF1) and the fourth finger (LF4),;
subdigital lamellae under the first toe (LT1) and the
fourth toe (LT4); precloacal pores (PP); and postcloacal
tubercles (PAT).
Molecular analyses: To confirm the taxonomic status of
the newly collected Goniurosaurus from Ha Long Bay,
Quang Ninh Province, a fragment of the mitochondrial
16S ribosomal gene was amplified, using the primer pair
16Sar and 16Sbr (Palumbi et al. 1991), for three samples
(VNMN 05424 plus two small tissue samples from
two released individuals, field numbers G8 and G12).
Tissue samples were taken from the tail tips, which were
disinfected before immediate release of the animals at the
site of capture. DNA was extracted from tissue samples
using the DNeasy blood and tissue kit, Qiagen (Redwood
City, CA). The extracted DNA from the fresh tissue
samples were amplified by PCR, with the PCR volume
(21ul) consisting of 10 ul of mastermix (Fermentas,
Canada), 5 ul of water, 2 ul of each primer at 10 pmol/
ul, and 2 wl of DNA. The PCR conditions were: 95 °C
for five minutes to activate the taq; with 40 cycles at 95
°C for 30s, 50 °C for 45s, 72 °C for 60s; and the final
extension at 72 °C for six minutes (Ngo et al. 2016).
PCR products were subjected to electrophoresis
through a 1% agarose gel (UltraPure™, Invitrogen). Gels
were stained for 10 minutes in 1x TBE buffer at 2 pg/
ml of ethidium-bromide, and visualized under UV light.
Successful amplifications were purified to eliminate
PCR components using GeneJET™ PCR Purifcation Kit
(Fermentas, Canada). Purified PCR products were sent to
lst Base (Selangor, Malaysia) for sequencing. Sequences
were edited using the program Geneious v.7.1.8 (Kearse et
al. 2012). After sequences were aligned using Clustal X v2
(Thompson et al. 1997), data were analyzed by Bayesian
inference as implemented in MrBayes v3.2 (Ronquist
et al. 2012). Settings for these analyses followed Le et
al. (2006), except that the number of generations in the
Bayesian analysis was increased to 1x10’. The optimal
model for nucleotide evolution was set to GTR+I+G as
selected by Modeltest v3.7 (Posada and Crandall 1998).
The cutoff point for the burn-in function was set to 13 in
the Bayesian analysis, as -InL scores reached stationarity
after 13,000 generations in both runs. Nodal support was
evaluated using posterior probability in MrBayes v3.2.
Uncorrected pairwise divergences were calculated in
PAUP*4.0b10 (Swofford 2001).
September 2019 | Volume 13 | Number 2 | e183
Goniurosaurus catbaensis in Ha Long Bay, Vietnam
72
Gekko gecko (AB028758)
Goniurosaurus kuroiwae (AB028766)
99 Goniurosaurus yingdeensis (KC900231)
Goniurosaurus zhelongi (KJ423105)
-Goniurosaurus araneus (AB308460)
Goniurosaurus luli (EU499390)
Goniurosaurus Iuii ML19 (MK041068)
53
73 Goniurosaurus luii TDLS2012.1 (MKO41069)
100
gut ee neunts luli (KC765083)
Goniurosaurus luli (KC 765084)
99 Goniurosaurus luli TAQ182 (MK041067)
92 26
Goniurosaurus luli IEBR3254 (MK041070)
Goniurosaurus liboensis (KC900230)
Goniurosaurus catbaensis (EU499389)
Cat Ba Island
él 100 || Goniurosaurus catbaensis VNMN05424 (MK041071)
91
Goniurosaurus catbaensis G8 (MK041072)
Other Islands
in Ha Long Bay
Goniurosaurus catbaensis G12 (MK041073)
100 Goniurosaurus lichtenfelderi (JF799756)
Goniurosaurus hainanensis (KC765080)
0.05
Fig. 2. Phylogram of Goniurosaurus based on the Bayesian analysis of a 16S ribosomal fragment. Numbers next to nodes are
Bayesian posterior probabilities. Voucher numbers of new samples and GenBank accession numbers are placed after species names
and in parentheses, respectively.
Species distribution models (SDMs): Based on
occurrence records and a set of 19 environmental factors,
the current overall availability of suitable habitats for G.
catbaensis were predicted using the program Maxent
Version 3.3.3.e (Beaumont et al. 2005; Phillips et al.
2006). Only the most distant occurrences of each site
were included in the analyses to minimize effects of
spatial autocorrelation and to ensure the independence
of the records (Jennings and Veron 2011; Jennings et al.
2013). As a result, 11 records were filtered from a total
of 60 localities of G. catbaensis on Cat Ba Island and
Ha Long Bay. Nineteen bioclimatic variables that were
obtained from the WorldClim global climate database
(http://www.worldclim.org, accessed September 2016;
Hijmans et al. 2005; Table 1) were used as environmental
predictors.
Threat records: To get a first impression of trade in
Goniurosaurus species in Vietnam, local pet markets
were visited in Hai Phong and Ho Chi Minh cities, the
two most important trade centers in the country, and
different Internet platforms were investigated. Two local
dealers from Ho Chi Minh City offering Goniurosaurus
online were interviewed in September 2016, in order
to trace the source of the traded Goniurosaurus species
Amphib. Reptile Conserv.
in Vietnam. Additionally, five fishermen from the Ha
Long Bay were interviewed to identify caves used by
tourism companies for night parties, and determine
the general attitude and use of the species in Ha Long
Bay. Those sites located within the World Heritage Site
were subsequently surveyed in July 2016 to evaluate
potential threats from tourism activities. The names of
interviewees are kept anonymous to ensure data privacy
rights and Internet links are not disclosed to prevent
misuse. Accurate locality data, cave names, and prices
are also not presented to prevent targeted poaching for
the wildlife trade.
Results
New records of Goniurosaurus catbaensis: During
the present study, new Goniurosaurus occurrences were
discovered on four small offshore islands, including two
tourism caves in Ha Long Bay, Quang Ninh Province.
The distances between these islands ranged from 1.4 km
to 13 km, while the shortest distance between Cat Ba
Island and one surveyed island in Ha Long Bay was 1.2
km. A total of 14 individuals (eight males, four females,
one juvenile, and one unsexed individual which was only
photographed) were recorded on these islands, which
September 2019 | Volume 13 | Number 2 | e183
Ngo et al.
Table 1. Bioclimatic variables from environmental data (Source: http://www.worldclim.org, accessed September 2016).
No. Bioclimatic variables from the WorldClim dataset
l BIO1 = “Annual Mean Temperature”
2 BIO2 = “Mean Diurnal Range" (Mean of monthly [max temp - min temp])
3 BIO3 = "Isothermality" (P2/P7) (*100)
4 BIO4 = "Temperature Seasonality" (standard deviation * 100)
5 BIO5 = "Max Temperature of Warmest Month"
6 BIO6 ="Min Temperature of Coldest Month"
7 BIO7 ="Temperature Annual Range" (P5—P6)
8 BIO8 = "Mean Temperature of Wettest Quarter"
9 BIO9 = "Mean Temperature of Driest Quarter"
10 BIO10 = "Mean Temperature of Warmest Quarter"
1] BIO11 ="Mean Temperature of Coldest Quarter"
12 BIO12 = "Annual Precipitation (year)"
13 BIO13 = "Precipitation of Wettest Month"
14 BIO14 = "Precipitation of Driest Month"
15 BIO15 = "Precipitation Seasonality" (Coefficient of Variation)
16 BIO16 = "Precipitation of Wettest Quarter"
17 BIO17 = "Precipitation of Driest Quarter"
18 BIO18 = "Precipitation of Warmest Quarter"
19 BIO19 = "Precipitation of Coldest Quarter"
ranged between 0.34 and 2.94 km? in size.
Molecular analysis using Bayesian inference of
the obtained matrix containing 613 aligned characters
showed that all samples from Cat Ba Island (n = 1) and
from the most distant other islands in Ha Long Bay (n=3)
clustered in a single clade with strong statistical support
(posterior probability = 100%, Fig. 2). Genetic analyses
revealed that sequences of the new records from Ha
Long Bay, Quang Ninh Province, were identical to each
other and virtually the same (99% to 100%) as that of the
holotype of G. catbaensis from Cat Ba Island (GenBank
accession number: EU499389). The maximum genetic
divergence between the samples is approximately 0.3%,
whereas the lowest divergence between two species of
this genus, i.e., G. hainanensis and G. lichtenfelderi, is
approximately 2.3% (Table 2). These results confirmed
the newly recorded Goniurosaurus populations in Ha
Long Bay are conspecific with G. catbaensis from Cat
Ba Island (Fig. 2).
In addition, the morphological characters of the newly
recorded G. catbaensis from Ha Long Bay accorded well
with the population from Cat Ba Island, except that three
of six individuals from a single site in Ha Long Bay
showed a postrostral (internasal) scale. This character 1s
consistently lacking 1n individuals recorded so far from
Cat Ba Island (Ziegler et al. 2008) [Fig. 3A, 3B; Table 3].
Microhabitat selection: A total of 61 sightings took
place (13 from smaller islands in the Ha Long Bay,
and 48 from Cat Ba Island). Goniurosaurus catbaensis
was active in the surroundings of large limestone caves
covered in part by primary forest vegetation and in the
vicinity of primary shrub vegetation on limestone. Mean
air temperatures were 28.1 + 1.7 °C (21.5-31.3 °C, n=
B
Long Bay. Photos H.N. Ngo.
Amphib. Reptile Conserv.
Fig. 3. Absence versus occasional presence of internasal scales of Goniurosaurus catbaensis from (A) Cat Ba Island and (B) Ha
September 2019 | Volume 13 | Number 2 | e183
Goniurosaurus catbaensis in Ha Long Bay, Vietnam
Forest
floor 5%
wo
Oo
o
NO
So
i=)
=
i=)
i=)
a4
£
‘)
hel
a]
=
D
®
<
Fig. 4. (A) Substrate selection of Goniurosaurus catbaensis. (B) Box plots of perch heights of different age classes and sexes.
59) slightly higher than mean substrate temperatures of
26.02 + 1.5 °C (22.2—28.2 °C, n= 28, Table 4). Recorded
relative humidity at microsites ranged between 70-99%
(mean 84.9 + 6.99%, n = 52).
A vast majority of lizards was found on limestone
cliffs (62%), followed by rocks (28%), while only a few
specimens were found on the forest floor (5%), branches
(3%), or sand (2%) [Fig. 4A]. A significantly lower
number of lizards was encountered inside compared
to outside of limestone caves (26.9% vs. 73.1%,
respectively). Goniurosaurus catbaensis selected spots
with a mean canopy coverage of 95.2 + 9.6% (n = 63,
Table 4). Adult specimens (non-gravid) were found at
average heights of 1.15 m (n = 38), while juveniles and
gravid females resided at significantly lower heights of
0.28 m(n=4) and 0.41 m (n= 12), respectively (t= 2.82,
df = 48, P < 0.05; t = 2.06, df = 40, P < 0.05, Fig. 4B).
A majority (about 77.4%, n = 48) of lizards was resting
during the surveys, while only a few individuals (n = 14)
were found actively foraging.
Suitable habitats for G. catbaensis were predicted to
encompass a majority of small islands belonging to Cat
Ba Island and Ha Long Bay, and include a wider area on
the coastal mainland of Quang Ninh Province, where no
surveys have been conducted so far (Fig. 5).
Trade: Trade in living tiger geckos has been frequently
recorded by our team in local pet markets from Hai
Phong and Ho Chi Minh cities, as well as on Facebook
since 2015. Interviews with two local traders in Ho Chi
Minh City revealed that they pay for local villagers living
within the species’ distribution range to collect live tiger
geckos during the non-hibernation season, confirming
the wild (rather than captive-bred) source of traded
animals. The dealers reportedly received individuals of
three tiger gecko species, namely G. huuliensis, G. luii,
and G. catbaensis, collected in April 2015. Among those,
three individuals of G. huuliensis (one male and two
females) were allegedly collected by a local hunter from
Huu Lien Nature Reserve, Lang Son Province. Two local
collectors from Cao Bang Province reportedly collected
six individuals (three males and three females) of G. /uii
in northern Vietnam and another local hunter collected
two couples of G. catbaensis. These 13 wild caught tiger
geckos were transferred to pet markets in Ho Chi Minh
City, southern Vietnam, in April 2015.
Human impacts on the habitat: Tourism activities in
the region have dramatically increased in the past, and
likely exerted enormous pressure on wild G. catbaensis
populations. Events organized by tourism companies
Table 2. Uncorrected (“p”) distance matrix showing percentage pairwise genetic divergence (16S) between members of
Goniurosaurus.
Species name 1 2 3 4 5 6 7 8 9
1. G. araneus —
2. G. catbaensis 6.4-6.7 -
3. G. hainanensis [3x 12.4-12.8 -
4. G. kuroiwae 20.4 19.5-19.8 1.3 —
5. G. liboensis 6.3 6.6-6.8 12.8 21.9 —
6. G. lichtenfelderi 12.9 11.2-11.6 23 18.8 13:3 —
7. G. luii 5.6-6.2 6.2-7.1 12.2-12.9 20.0-204 3.43.8 11.5-13.5 —
8. G. yingdeensis 14.8 13.4-13.5 15.2 18.8 13.0 Las2 13.3-13.5 —
9. G. zhelongi 15.3 14.2-14.4 16.9 21.4 13.4 16.2 14.8-15.4 48 —
Amphib. Reptile Conserv. 6 September 2019 | Volume 13 | Number 2 | e183
Ngo et al.
106°30'0"E 107°O'0"E
107°30'0"E 108°0'0"E
21°30'0"N
21°0'0"N
21°30'0"N
21°0'0"N
Legend
===== National boundary
Province boundary
Habitat suitability
*
——— Low
20°30'0"N
106°30'0"E 107°0'0"E
0 15 30
20°30'0"N
107°30'0"E
60 Kilometers
108°0'0"E
Fig. 5. Predicted habitat suitability for Goniurosaurus catbaensis in Vietnam.
regularly took place in at least two caves located
within the UNESCO World Heritage Site. According to
interviews with fishermen, daily excursions to the caves
are scheduled to start at 7:30 PM and end around 11:00
PM. On these occasions, tourists dine in brightly lit
caves before returning to their tour boats (Fig. 6B). As
a consequence, wildlife is likely to be disturbed by the
candle light, noisy sounds, and waste left by the tourists.
Discussion
New population records: Since its discovery in 2008,
the Cat Ba Tiger Gecko was thought to be endemic to
Cat Ba Island (Ziegler et al. 2008). These new records
of G. cf. catbaensis on further offshore islands in Ha
Long Bay confirmed for the first time the occurrence of
the species outside its type locality. The newly recorded
specimens showed an insignificant genetic divergence
from the type series from Cat Ba Island and could be
assigned to G. catbaensis (Table 2). Accordingly, the
newly collected specimens from Ha Long Bay were also
almost identical to the type series of G. catbaensis in
morphology, except for the presence of a single internasal
scale (which 1s absent in the type series from Cat Ba, see
Ziegler et al. 2008) in a few individuals from a single
site in Ha Long Bay. These findings indicated a slightly
broader distribution range of the species than previously
expected.
According to Li et al. (2010), the islands of Ha Long
Bay and Cat Ba Archipelago were shaped by the erosion
of limestone karst formations within the Gulf of Tonkin
Amphib. Reptile Conserv.
at the northern east coast of Vietnam after the coastal
shelf region became inundated by marine waters about
13,000 years ago. Repeated falls (> 50 m) of the sea
level during glaciations periodically connected various
islands and the mainland, which allowed exchanges
between island and mainland populations, as well as
colonization and re-colonization between island and
mainland populations (Li et al. 2010; Liang et al. 2018).
Thus, past recurrent gene flow is assumed to have
occurred between (sub)populations, which helped to
maintain a classical island-mainland metapopulation—in
accordance with the high genetic similarity between G.
catbaensis (sub)populations from different islands with
identical habitats (Hanski 1991; Harrison and Taylor
1997; Levins 1969). Orlov et al. (2008) confirmed
that G. lichtenfelderi was found from both continental
mainland and islands. On the other hand, Liang et al.
(2018) suggested that G. lichtenfelderi diverged from
G. hainanensis of Hainan Island to Vietnam (including
both mainland and island populations), which might have
occurred during the glacial periods with past dispersal
events. The speciation in the diversification process of
Goniurosaurus was probably promoted by the adaption to
different microhabitats. Populations of G. lichtenfelderi
were found on granite beds of valley streams, while the
closely related G. hainaensis is found on igneous rocks
and G. catbaensis occurs in karst forests (Orlov et al.
2008; Liang et al. 2018; Ziegler et al. 2008; Nguyen et
al. 2018).
To avoid the misuse of distribution data for targeted
harvesting of the species (e.g., Lindenmayer and Scheele
September 2019 | Volume 13 | Number 2 | e183
Goniurosaurus catbaensis in Ha Long Bay, Vietnam
Table 3. Morphological characters of Goniurosaurus from Ha Long Bay, Quang Ninh Province, compared with G. catbaensis from
Cat Ba Island, Hai Phong Province. Measurements are given in mm. Note: (*) n= 6; (*)n=2.
Specimens
SVL
TaL
IN
PostIN
PM
GP
CIL
MB
GST
TL
DTR
LF1
LF4
LT1
LT4
PP
PAT
2017; Stuart et al. 2006; Yang and Chan 2015), detailed
locality information of the new records is being withheld.
According to the SDMs G. catbaensis is predicted to
occur on other, similar islands in the Gulf of Tonkin, but
Ha Long Bay (current study, n = 13)
74.54-122.7 (111.2 + 11.9)
10.1-97.6 (69.9 +27)
33.9-60.2 (52.9+6.5)
21.3-33.8 (30.2 +2.9)
14.4-24.56 (22.1 + 2.5)
7.1-14.9 (12.8 + 1.9)
32.2-53.8 (50.4+ 5.6)
42-67.47 (60.1 + 6.2)
8.7-13.4 (11.9 + 1.1)
9.4-13.2 (10.8 + 1.5)*
5.6-8.3 (7.5 +0.7)
2.8-5.3 (4.01 + 0.8)
3.39-4.33 (3.9 + 0.34)*
6.78-8.62 (7.98 + 0.67)*
11.8-15.03 (13.9 + 1.23)*
12.3-10.8 (18.1 +2.1)
27.6-32.5 (29.9 + 1.7)*
3.5-3.8 (3.68 + 0.1)
1.9-2.3 (2.140.1)
1.28-1.48 (1.37 + 0.05)
2.3-3.01 (2.35 + 1.6)
0.9-1.2 (1.1 £0.1)*
9-10 (9.4 +0.5)*
8-9 (9.75 + 0.45)*
5-6 (5.25 + 0.5)
0-1 (0.23 + 0.4)
0-2 (0.4 + 0.77)
2-3 (2.5+0.7)8
7
45-49 (46.75 + 1.7)"
104-109 (106.5 + 3.5)"
9-12 (10.5+1.3)8
35-37 (36 + 1.4)"
234
9-12 (10.25 + 1.3)"
18-19 (18.75 + 0.5)"
9-10 (9.75 + 0.5)
240
20-24 (22.5 +1.4)*
1-3 (2.25 + 0.6)*
Amphib. Reptile Conserv.
Cat Ba Island (current study, n = 48)
69.2-130.4 (108.9 + 12.6)
28.9-104.02 (78 + 17.7)
43.07-58.43 (48.44 5.4)*
17.8-34.2 (29.8 + 3.5)
13.9-28.2 (21.9 +2.5)
8.2-16.9(12.4+ 1.9)
29.7-54 (47.8 + 4.7)
36.2-65 (57.9 + 5,99)
10.45-13.4 (12.1 + 1.0)*
9.78-12.13 (11.1 + 0.88)*
6.1-8.95 (7.6 + 1.1)*
2.8-4.3 (3.540.5)*
2.9-4.2 (3.74 0.5)*
6.9-8.47 (7.5 + 0.6)*
11.9-15.1 (13.1 +1.3)*
15.5-19.5 (17.2 + 1.4)*
26.6-32.8 (29.2 +2.5)*
3.3-4.3 (3.74 0.2)
2.04-2.45 (2.3 +0.14)*
1.1-1.5 (1.36 + 0.09)
1.79-3.3 (2.4+ 0.4)
1.07-1.1 (1.09 + 1.14)*
8-11 (10.08 + 1.1)*
8-10 (8.8 +0.7)*
6-8 (7+ 0.47)*
0
0
2-3 (2.83 + 0.41)*
6-9 (7.8+1.2)*
41-56 (47.8 + 4.4)*
102-109 (103.8 + 3.8)*
9-14 (10.3 + 1.6)*
27-34 (31.5 + 3.0)*
19-25 (22.3 + 1.97)*
9-11 (10 +0.7)*
19-20 (19.3 + 0.5)*
9-10 (9.91 +0.3)*
22-24 (23.4 + 0.8)*
21*
2-3 (2.5+40.5)*
Cat Ba Island (Ziegler et al. 2008) [n = 4]
84.7-111.5 (102.4 + 14.5)
§2.5-101.5 (68.1 + 27.6)
23.1-30.6 (27.7 +4.1)
16.2-21.6 (19.5 +2.9)
10.1-14.3 (12.2 + 2.0)
9.8-12.6 (11.5 + 1.6)
8.5-12.3 (10.6 +2.1)
3.61-3.67 (3.7 + 0.05)
1.43-2.11 (1.6 +0.4)
2.29-2.43 (2.33 + 0.07)
1.02-1.15 (1.09 + 0.07)
8-9 (8.7 + 0.5)
6-8 (7.8 + 0.6)
5-6 (5.1 40.4)
0
0
2-3 (2.8 + 0.5)
6-7 (7.22 + 0.6)
52-55 (54.0+ 1.1)
112-127 (119.2 + 7.6)
8-11 (9.8 + 1.6)
33-34 (33.7 + 0.6)
23-25 (24.0 + 1.2)
11-12 (11.75 + 0.5)
18-19 (18.1 +£0.5)
11-12 (11.44 0.6)
22-24 (23.440.7)
5-21 (15.3 +2.5)
2-3 (2.8 + 0.5)
is still endemic to Ha Long Bay and Cat Ba Archipelago.
According to Orlov et al. (2008) the type locality of
G. lichtenfelderi is an offshore island in Bai Tu Long
Archipelago, which is contiguous with Ha Long Bay
September 2019 | Volume 13 | Number 2 | e183
Ngo et al.
-
—see i _
Fig. 6. Potential threats to Goniurosaurus. (A) Flooding of Viet Hai Commune in August 2015. (B) Tourist event in a cave within
B
the UNESCO World Heritage Site on Ha Long Bay. Photos H.N. Ngo.
in the Gulf of Tonkin. However, extensive field surveys
have failed to record any individual of G. catbaensis,
occurring in syntopy with G. lichtenfelderi (Gawor et al.
2016; Nguyen et al. 2011; Orlov et al. 2008). The habitat
of G. lichtenfelderi in Bai Tu Long was described as
valleys of forest streams on granite rocks within mixed
forests of bamboo and broad-leaved trees (Gawor et al.
2016; Nguyen et al. 2009; Nguyen et al. 2011; Orlov et
al. 2008; Ziegler et al. 2008), while G. catbaensis was
found only in limestone karst ecosystems present in Ha
Long and Cat Ba archipelagos. Accordingly, our SDMs
predicted the potential distribution of G. catbaensis to
encompass Ha Long Bay and Cat Ba Archipelago, but
excluding Bai Tu Long Archipelago (Fig. 5). However,
the present SDMs also predicted the mainland area
including limestone formations around Ha Long City to
be suitable for G. catbaensis. Thus, it will be important to
search for further occurrences at these predicted sites in
order to determine the exact distribution boundaries, and
to assess genetic diversity of potentially new populations.
Microhabitat selection: Both sex- and age-related
perch selection were found in G. catbaensis, namely
differences in perch heights. Specifically, juveniles and
gravid females occurred at significantly lower heights
than subadults and adults. Similar habitat divergences
between juveniles and adult individuals have been
reported for Crocodile Lizards in Vietnam (van Schingen
et al. 2015), and gekkonids in New Caledonia (Snyder et
al. 2010).
This study also revealed that the body surface
temperature of G. catbaensis showed a highly positive
correlation with the air temperature (7, = 0.56; P < 0.05,
n = 23) and substrate temperature (7, = 0.66; P < 0.001,
n= 26). Thus, as in other ectotherms, basic physiological
functions of G. catbaensis, such as locomotion, growth,
and reproduction are determined by the environmental
temperature. Since tropical lizards are considered to
have narrow temperature optima, and only few options
for behavioral and physiological compensation, they
are assumed to be especially vulnerable to extinction by
climate warming (Deutsch et al. 2008; Doody and Moore
2010; Huey et al. 2009; Vié et al. 2009). In particular,
body surface temperatures of G. catbaensis ranged from
between 23.6 and 30.6 °C (mean = 27.2 + 1.6 °C, n= 26)
and were comparably higher than those of G. kuroiwae
with average skin surface temperatures of 16.6 °C in the
humid subtropical Oriental forest (Werner et al. 2005).
Potential threats and recommendations for
conservation: Due to the restricted distribution range,
low densities, and estimated global population being
much lower than suggested threshold values for minimal
viable populations, the Cat Ba Tiger Gecko is expected
to be especially endangered to unsustainable for harvest
(Ngo et al. 2016). Consequently, the species was recently
assessed and ranked by the IUCN Red List of Threatened
Species as "Endangered" (Nguyen et al. 2016). Other
members of the genus Goniurosaurus from Vietnam
have not been considered for inclusion on the IUCN
Red List yet, as data on their population statuses are
currently lacking. The findings reported here indicate
that not only G. catbaensis, but also G. huuliensis and
G. luii, are subject to intensive collection for local trade
and provide concrete evidence for the wild source of
the respective specimens. It is likely that the reported
Table 4. Environmental parameters characterizing the microhabitat selection of Goniurosaurus catbaensis.
Parameter Number of sightings (n)
Canopy cover [%] 63
Height [m] 54
Elevation [m asl] 60
Air Temperature [°C] 59
Substrate Temperature [°C] 28
Relative air Humidity [%] 52
Amphib. Reptile Conserv.
Min Max Mean + SD
50 100 95.2+9.6
0 3 0.97 + 0.86
4 132 46.2 + 32.9
21-8 313 28.1+1.7
222 28.2 26.02 + 1.5
70 99 84.9 + 6.99
September 2019 | Volume 13 | Number 2 | e183
Goniurosaurus catbaensis in Ha Long Bay, Vietnam
cases only reflect a small proportion of illegal harvesting
activities. Since over-exploitation of local populations
of range-restricted lizard species has been repeatedly
found to rapidly cause extinction (e.g., Aultya et al.
2016; Stuart et al. 2006; Yang and Chang 2015), further
research on the population status, distribution, ecology,
and availability of suitable microhabitat sites is critically
needed. The results of such studies may lead to the
elevation or determination of the conservation status of
other tiger gecko species and provide critical scientific
data for future captive breeding programs. To reduce
poaching and to control the trade in wild Goniurosaurus,
we recommend continued monitoring of the scales and
patterns of trade in combination with aforementioned
population assessments. We also strongly advise
against providing exact locality information for new
Goniurosaurus populations in future publications, as this
action might increase poaching activities at respective
sites (Lindenmayer and Scheele 2017; Stuart et al. 2006;
Yang and Chan 2015).
In addition to the illegal collection of animals, human
impacts on habitats have dramatically increased by
means of expanding tourism activities (see also Ngo et
al. 2016). Tourism events in caves, causing disturbance
by candle light, noisy sounds, and waste might result in
the extirpation of G. catbaensis within these limestone
caves. We suggest that tourism companies should hold
such events only on their boats to reduce disturbances
in the cave habitats of G. catbaensis, or at least restrict
tourist access to only limited, selected islands.
Following Ngo et al. (2016), the sites in Viet Hai
Village on Cat Ba Island had been recommended as a
priority conservation zone for species conservation,
since G. catbaensis was found to be most abundant at
those sites. However, during the most recent survey in
July 2016, no specimens of G. catbaensis were observed
in Viet Hai Commune. We assume that an extensive flood
in August 2015 might have killed a large amount of the
local wildlife, including the Cat Ba Tiger Gecko, at this
site. Viet Hai Commune was isolated for a week after
torrential rains brought the water level up to the roofs of
local houses. Since G. catbaensis was found to generally
occur at low elevation ranges (4-132 m asl), and Viet
Hai is situated only up to 36 m asl (see Fig. 6B), this
species is particularly vulnerable to natural catastrophes
such as storms, floods, and sea level rises, throughout
its distribution range (see Dessler 2016; Saunders et al.
1991). Since local populations are extremely small, they
are especially prone to extinction by catastrophic events.
The devastating consequences of such natural disasters
underline the importance of maintaining numerous
independent subpopulations in order to compensate for
such events.
In summary, the insular (sub)populations of G.
catbaensis are threatened by harvest for the pet trade,
human activities within its habitats, and natural
catastrophes such as increasingly extreme floods and
storms in northeastern Vietnam, probably triggered
by climate change (The Governmental Committee on
Flood and Storm Prevention 2016). Thus, we herewith
emphasize the importance of setting aside priority
conservation zones for this species, in order to establish
Amphib. Reptile Conserv.
a connected and buffered system that allows (sub)
populations to recover from catastrophes. We also
recommend the establishment of an assurance population,
i.e., an ex situ conservation breeding program for the
species. Although such an effort has been started at the
Me Linh Station for Biodiversity (see Ziegler et al. 2016)
in Northern Vietnam, more resources need to be allocated
to enhance the effort to conserve the species.
Acknowledgements.—For supporting field work and
issuing relevant permits, we thank the authorities of the
Cat Ba National Park (CBNP), Hai Phong City, and the
Management Department of Ha Long Bay (MDHLB),
Quang Ninh Province. We are very thankful to L. Barthel
(University of Cologne) and K.X. Nguyen (CBNP) for
assistance in the field. We are grateful to T. Pagel and C.
Landsberg (Cologne Zoo); M. Bonkowski (University of
Cologne); C.X. Le, T.H. Tran, T.H. Vu, C.T. Pham, and
T.V. Nguyen (IEBR, Hanoi); M.T. Nguyen, L.V. Vu, and
T.T. Nguyen (VNMN, Hanoi); and V.Q. Luu (VNUF, Ha
Noi) for their support of conservation-based biodiversity
research in Vietnam. Thanks to H.T. Ngo for laboratory
assistance. Our research was funded by Cologne Zoo, the
Mohamed bin Zayed Species Conservation fund (Project:
170515492), the National Foundation for Science and
Technology Development (NAFOSTED, Grant No. 106-
NN.06-2016.59), the Idea Wild, and Vietnam National
Museum of Nature (VNMN). Cologne Zoo is a partner of
the World Association of Zoos and Aquariums (WAZA):
Conservation Project 07011 (Herpetodiversity Research).
Research of Hai Ngoc Ngo in Germany is funded by the
German Academic Exchange Service (DAAD).
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Ngo et al.
Hai Ngo Ngoc is a Ph.D. candidate at the Institute of Zoology, University of Cologne, and the Cologne
Zoo, Germany. He has worked as a researcher at the Vietnam National Museum of Nature since 2014,
and finished his M.Sc. degree in 2015 from the University of Science, Vietnam National University,
Hanoi. Hai has participated in diverse herpetological surveys in Vietnam and has experience in field
research and conservation work. His focus is on the ecology, phylogeny, and conservation of endemic
and endangered reptile species in Vietnam.
Tuan Quang Le is a researcher at the Institute of Ecology and Biological Resources (IEBR), Vietnam
Academy of Science and Technology (VAST). He is conducting Ph.D. research at Academia Sinica,
Taiwan, and majored in ecology, ecological modeling, and remote sensing. His current research
focuses on the application of remote sensing and geographical information systems in the ecology
and ecological modeling of mammals and reptiles. In particular, Tuan is using species distribution
modeling to predict the potential distributions of species, including reptiles and mammals, in Vietnam.
In addition, he evaluates the impacts of climate change on those species based on future climate
scenarios, and is also developing remote sensing-based approaches for mapping species habitats
Minh Le Pham is a researcher at the Ha Long Bay Management Department. He finished his M.Sc.
degree in 2018 at the Vietnam National University, Hanoi. His work focuses on the ecology and
conservation of biodiversity and landscapes in the Ha Long Bay World Heritage Site.
Truong Quang Nguyen is a researcher at the Institute of Ecology and Biological Resources (IEBR),
Vietnam Academy of Science and Technology (VAST), and is a member of the Biodiversity and Nature
Conservation projects of the Cologne Zoo. Truong finished his Ph.D. in 2011 at the Zoological Research
Museum Alexander Koenig (ZFMK) and the University of Bonn, Germany, as a DAAD Fellow. From
2011 to 2014, he worked as a postdoctoral student in the Zoological Institute, University of Cologne.
Truong has conducted numerous field surveys and is the co-author of 12 books and more than 300
papers related to biodiversity research and conservation in Southeast Asia. His research interests focus
on the systematics, ecology, and phylogeny of reptiles and amphibians from Southeast Asia.
Minh Duc Le has been working on conservation-related issues in Southeast Asia for more than 15
years. His work focuses on biotic surveys, wildlife trade, and conservation genetics of various wildlife
groups in Indochina. Minh is currently working on projects which characterize genetic diversity
of highly threatened reptiles and mammals in the region, and he has pioneered the application of
molecular tools in surveying critically endangered species in Vietnam. He has long been involved in
studying the impact of the wildlife trade on biodiversity conservation in Vietnam, and is developing a
multidisciplinary framework to address this issue in the country.
Mona van Schingen finished her Ph.D. on the Vietnamese Crocodile Lizard in 2017 at the Institute
of Zoology of the University of Cologne and the Cologne Zoo, Germany. Since 2011, Mona has been
investigating the herpetofauna of Vietnam, in the working group of Thomas Ziegler. She has conducted
diverse field excursions to Vietnam and is engaged in several research, conservation, and awareness
projects focusing on various species in Vietnam. Since 2017 she has been working for the German
CITIES Scientific Authority at the Federal Agency for Nature Conservation.
Thomas Ziegler has been the Curator of the Aquarium/Terrarium Department of the Cologne Zoo
since 2003, and is the coordinator of the Cologne Zoo’s Biodiversity Research and Nature Conservation
Projects in Vietnam and Laos. Thomas studied biology at the University Bonn (Germany), and
conducted his diploma and doctoral thesis at the Zoological Research Museum Alexander Koenig
in Bonn, with a focus on zoological systematics and amphibian and reptile diversity. Thomas has
been engaged with herpetological diversity research and conservation in Vietnam since 1997. As a
zoo curator and project coordinator, he tries to combine in situ and ex situ approaches—viz., to link
zoo biological aspects with diversity research and conservation in the Cologne Zoo, as well as in
rescue stations and breeding facilities in Vietnam and in Indochina’s last remaining forests. Thomas is
a professor at the Institute of Zoology of Cologne University. Since 1994, he has published more than
430 papers and books, mainly dealing with herpetological diversity.
Amphib. Reptile Conserv. 13 September 2019 | Volume 13 | Number 2 | e183
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 14—27 (e187).
urn:lsid:zoobank.org:pub:7F259D5F-3CBF-4421-BA54-5CECDB687340
A new species of dwarf day gecko (Reptilia: Gekkonidae:
Cnemaspis) from lower-elevations of Samanala Nature
Reserve in Central massif, Sri Lanka
1*Suranjan Karunarathna and 7Kanishka D.B. Ukuwela
'Nature Explorations and Education Team, No: B-1 / G-6, De Soysapura Flats, Moratuwa 10400, SRI LANKA *Department of Biological Sciences,
Faculty of Applied Sciences, Rajarata University of Sri Lanka, Mihintale 50300, SRI LANKA
Abstract.—A new day gecko species of genus Cnemaspis Strauch, 1887 is described from a midland forested
area of Udamaliboda (north-western foothills of Samanala Nature Reserve) in Sri Lanka. This species is
medium in size (30-35 mm SVL) and can be differentiated from all other Sri Lankan congeners by a suite
of distinct morphometric, meristic, and color characters (dorsum with smooth and homogeneous granular
scales; chin, gular, pectoral, and abdominal scales smooth; precloacal pores absent in males, 14—15 femoral
pores separated by 9-11 unpored interfemoral scales in males; subcaudals smooth, subhexagonal, enlarged,
subequal, forming a regular median row). It was recorded from tall trees with smooth bark in home gardens,
and also on clay walls in very old tall houses in wet, cool, and shady forests, distributed across mid elevations
(~450-—650 m) with limited anthropogenic disturbance. They can climb to heights of 7 m on vertical surfaces of
trees. The most noteworthy behavior of this species is that when “scared,” it runs only upward to the canopy
of the tree or along the wall to hide within crevices. The major threats for this species in Udamaliboda and other
locations in lower Samanala Nature Reserve are habitat loss due to expansion of commercial-scale agriculture
and monoculture plantations, and illicit forest encroachments. Therefore, these foothill forests warrant special
conservation, habitat protection, further in-depth research, and specific hands-on management practices.
Keywords. Arboreal, conservation, ecology, rainforest, redlist, taxonomy, Sripadha, threats
Citation: Karunarathna S, Ukuwela KDB. 2019. A new species of dwarf day gecko (Reptilia: Gekkonidae: Cnemaspis) from lower-elevations of
Samanala Nature Reserve in Central massif, Sri Lanka. Amphibian & Reptile Conservation 13(2) [General Section]: 14-27 (e187).
Copyright: © 2019 Karunarathna and Ukuwela. This is an open access article distributed under the terms of the Creative Commons Attribution
License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and
reproduction in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will
be duly enforced, are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 16 May 2019; Accepted: 29 July 2019; Published: 9 September 2019.
Introduction
Sri Lanka’s wet zone, home to unique assemblages of
floral and faunal communities with high endemism, is
one of the smallest biodiversity hotspots in the world
(Meegaskumbura et al. 2002; Gunawardene et al. 2007).
Within the diverse reptile community of the island (~225
species), the diversity of geckos (family Gekkonidae) 1s
remarkable; 54 species (in eight genera) have been de-
scribed so far, accounting for 24% of the overall reptilian
species richness (Somaweera and Somaweera 2009; de
Silva and Ukuwela 2017). Of these, 44 species (~81%)
are endemic and 45 species (~83%) are threatened (MoE-
SL 2012, Karunarathna et al. 2019a,b). The genus Cne-
maspis comprises 32 species in Sri Lanka and all of them
are endemic (Batuwita et al. 2019; Karunarathna et al.
2019a,b; de Silva et al. 2019). Sri Lankan Cnemaspis
Correspondence. * suranjan.karu@gmail.com
Amphib. Reptile Conserv.
Species represent two distinct evolutionary lineages,
the C. kandiana and C. podihuna clades (Agarwal et al.
2017; Karunarathna et al. 2019b). The high species rich-
ness in Sri Lanka may be due to multiple possible colo-
nization events from the Indian mainland with isolated in
situ speciation (Agarwal et al. 2017).
During the past decade, the number of species recog-
nized in the genus Cnemaspis globally has grown rap-
idly, reaching over 150 species (Grismer et al. 2014; Uetz
et al. 2019; Karunarathna et al. 2019b), and Cnemaspis
is now the second most speciose gecko genus in the Old
World (Rosler et al. 2019). Though Sri Lanka is a small
island, it harbors about 21% of the world’s Cnemaspis
species, of which 90% have been described in the last two
decades, including many described only recently (Ka-
runarathna et al. 2019b). However, most of the Cnemas-
pis species from the dry and intermediate climatic zones
September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
of Sri Lanka are restricted to small isolated hillocks scat-
tered in the lowlands (Karunarathna et al. 2019b). Future
studies on the biogeography of Cnemaspis in Sri Lanka
are expected to highlight the importance of these isolated
habitats in generating and maintaining the diversity of
these unique groups of geckos on the island. During a
field excursion to Udamaliboda (northwest Samanala
Nature Reserve), an unidentified Cnemaspis species was
discovered that closely resembles C. gemunu, C. godage-
darai, C. phillipsi, and C. scalpensis, and it is described
here as a new species.
Materials and Methods
Specimen collection. Museum acronyms follow Sabaj
Pérez (2015). The type material discussed in this pa-
per is deposited in the National Museum of Sri Lanka
(NMSL), Colombo. Specimens were hand-caught and
photographed in life. Three specimens were euthanized
using halothane, fixed in 10% formaldehyde for two
days, washed in water, and transferred to 70% ethanol
for long-term storage. Tail tips were collected (as tissue
samples) before fixation in formaldehyde for future ge-
netic analyses and stored in 95% ethanol under relatively
cool conditions (20-25 °C). For comparison, we exam-
ined 402 Cnemaspis specimens (catalogued and uncata-
logued) representing all recognized Sri Lankan species,
including all type specimens housed at the NMSL and
The Natural History Museum, London (BMNH). Speci-
mens that formerly belonged to the Wildlife Heritage
Trust (WHT) collection and bear WHT numbers are cur-
rently deposited in the NMSL, catalogued under their
original numbers. Original specimens in this study were
collected during a survey on lizards of Sri Lanka under
permit numbers WL/3/2/1/14/12 and WL/3/2/42/18 (A
and B), issued by the Department of Wildlife Conserva-
tion, and permit numbers FRC/5 and FRC/6, issued by
the Forest Department of Sri Lanka. Additional informa-
tion on morphology and natural history of Sri Lankan
Cnemaspis species was extracted from the relevant lit-
erature (Bauer et al. 2007; Manamendra-Arachchi et
al. 2007; Wickramasinghe and Munindradasa 2007; Vi-
danapathirana et al. 2014; Amarasinghe and Campbell
2016; Wickramasinghe et al. 2016; Batuwita and Udu-
gampala 2017; Agarwal et al. 2017; Batuwita et al. 2019;
Karunarathna et al. 2019b). Assignment of unidentified
specimens to species was based on the presence of shared
morphometric and meristic characters (Wickramasinghe
et al. 2016; Batuwita and Udugampala 2017; Agarwal et
al. 2017; Batuwita et al. 2019; Karunarathna et al. 2019b;
de Silva et al. 2019).
Morphometric characters. Forty morphometric mea-
surements were taken (to the nearest 0.1 mm) using a Mi-
tutoyo digital Vernier calliper, and detailed observations
of scales and other structures were made through Leica
Wild M3Z and Leica EZ4 dissecting microscopes. The
Amphib. Reptile Conserv.
following symmetrical morphometric characters were
taken on the left side of the body: eye diameter (ED),
horizontal diameter of eye ball; orbital diameter (OD),
greatest diameter of orbit; eye to nostril length (EN), dis-
tance between anteriormost point of orbit and posterior
border of nostril; snout length (ES), distance between an-
teriormost point of orbit and tip of snout; snout to nostril
length (SN), distance between tip of snout and anterior-
most point of nostril; nostril width (NW), maximum hori-
zontal width of nostrils; eye to ear distance (EE), distance
between posterior border of eye and anteriormost point
of ear opening; snout to axilla distance (SA), distance be-
tween axilla and tip of snout; ear length (EL), maximum
length of ear opening; interorbital width (IO), shortest
distance between left and right supraciliary scale rows;
inter-ear distance (IE) distance across head between the
two ear openings; head length (HL), distance between
posterior edge of mandible and tip of snout; head width
(HW), maximum width of head between the ears and the
orbits; head depth (HD), maximum height of head at lev-
el of eye; jaw length (JL), distance between tip of snout
and corner of mouth; internarial distance (IN), smallest
distance between inner margins of nostrils; snout to ear
distance (SED), distance between tip of snout and ante-
riormost point of ear; upper-arm length (UAL), distance
between axilla and angle of elbow; lower-arm length
(LAL), distance from elbow to wrist with palm flexed;
palm length (PAL), distance between wrist (carpus) and
tip of longest finger excluding the claw; length of digits
I-V of manus (DLM), distance between juncture of the
basal phalanx with the adjacent digit and the tip of the
digit, excluding the claw; snout-vent length (SVL), dis-
tance between tip of snout and anterior margin of vent:
trunk length (TRL), distance between axilla and groin;
trunk width (TW), maximum width of body; trunk depth
(TD), maximum depth of body; femur length (FEL), dis-
tance between groin and knee; tibia length (TBL), dis-
tance from knee to ankle with heel flexed; heel length
(HEL), distance between ankle (tarsus) and tip of longest
toe (excluding the claw) with both foot and tibia flexed;
length of pedal digits I-V (DLP), distance between junc-
ture of basal phalanx with the adjacent digit and the digit
tip, excluding the claw; tail length (TAL), distance be-
tween anterior margin of the vent and tail tip; tail base
depth (TBD), maximum height of tail base; and tail base
width (TBW), widest point of tail base.
Meristic characters. Twenty-nine discrete characters
were observed and recorded using Leica Wild M3Z and
Leica EZ4 dissecting microscopes on both left and right
sides of the body (reported in the form L/R): numbers of
supralabials (SUP) and infralabials (INF), between first
labial scale and corner of the mouth; number of inter-
orbital scales (INOS), between left and right supracili-
ary scale rows; number of postmentals (PM) bounded by
chin scales, 1‘ infralabial on left and right and the men-
tal; number of chin scales (CHS), scales touching medial
September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
— 600m
— 1200m
Arid Zone
| Dry zone
Bi Intermediate zone
| Wet zone
| | Montane Forest
50
Kilometers
WGS 1984 UTM Zone 44N
Fig. 1. Currently known distribution of Cnemaspis anslemi
sp. nov. (Udamaliboda-star), and related species: C. phillipsi
(Gammaduwa-traingle), C. scalpensis (Gannoruwa—square),
C. gemunu (Haggala-—circle), and C. godagedarai (Ensalwatte—
diamond) in Sri Lanka.
edge of infralabials and mental between juncture of 1*
and 2™ infralabials on left and right; number of suprana-
sal (SUN), scales between nares; presence of postnasal
(PON), scales posterior to naris; presence of internasal
(INT), scale between supranasals; number of supraciliary
scales (SUS), above eye; number of scales between eye
and tympanum (BET), from posteriormost point of orbit
to anteriormost point of tympanum; number of canthal
scales (CAS), number of scales from posteriormost point
of naris to anteriormost point of the orbit; total lamel-
lae on manus I-V (SLM), counted from first proximal
enlarged scansor greater than twice width of largest palm
scale, to distalmost lamella at tip of digits; number of
dorsal paravertebral granules (PG), between pelvic and
pectoral limb insertion points along a straight line im-
mediately left of vertebral column; number of midbody
scales (MBS), from center of mid-dorsal row diagonal-
ly toward ventral scales; number of midventral scales
(MVS), from first scale posterior to mental to last scale
anterior to vent; number of belly scales (BLS), across ven-
ter between lowest rows of granular dorsal scales; total
Amphib. Reptile Conserv.
lamellae on pes I-V (SLP), counted from first proximal
enlarged scansor greater than twice the width of largest
heel scale, to distalmost lamella at tip of digits; number
of femoral pores (FP), present on femur; number of non-
pored posterior femoral scales (PFS), counted from distal
end of femoral pore row to knee; and interfemoral scales
(IFS), number of non-pored scales between first femoral
pores on both femurs. In addition, the texture (smooth
or keeled) of ventral scales, the texture (homogeneous
or heterogeneous) of dorsal scales, the number of spi-
nous scales on flanks (FLSP), and characteristics such as
appearance of caudal scales (except in specimens with
regenerated tails) were also recorded. Coloration was
determined from digital images of living specimens and
also from direct observations tn the field.
Natural history. The new species described here was
collected on a field survey conducted in Udamaliboda,
Samanala Nature Reserve of Sri Lanka (Fig. 1). Be-
havioral and other aspects of the natural history of the
focal species were observed through opportunistic and
non-systematic means. Such observations were made
at a minimum distance of 2-4 m from the focal animals
while taking precautions to avoid disturbances. To record
elevation and georeference species locations, an eTrex®
20 GPS (Garmin) was used. Sex was determined by the
presence (male) or absence (female) of femoral pores.
The conservation status of the species was evaluated us-
ing the 2001 IUCN Red List Categories and Criteria ver-
sion 3.1 (UCN 2012).
Systematics
Cnemaspis anslemi sp. nov.
urn:Isid:zoobank.org:act: A5B58BCF-0BEE-4714-971 B-B38218F74956
Anslems’ Day Gecko (English)
Anslemge divaseri hoona (Sinhala)
Anslemvin pahalpalli (Tamil)
Figs. 2-5; Tables 1-2
Holotype. NMSL.2019.14.01, adult male, 34.4 mm SVL
(Fig. 2), collected from a tall, straight tree with good
canopy cover in a home garden (bordering forest) in
Udamaliboda, Kegalle District, Sabaragamuwa Province,
Sri Lanka (6.859728°N, 80.448736°E, WGS1984;
elevation 485 m, around 16.00 hrs) on 25 March 2019 by
Suranjan Karunarathna and Kanishka Ukuwela.
Paratypes. NMSL.2019.14.02, adult female, 32.5 mm
SVL collected from an old clay house wall (bordering
forest) in Udamaliboda, Kegalle District, Sabaragamuwa
Province, Sri Lanka (6.869611°N, 80.457069°E,
WGS1984; elevation 634 m, around 10.00 hrs) on 26
March 2019 by Suranjan Karunarathna and Kanishka
Ukuwela, and NMSL.2019.14.03, adult female, 30.0 mm
SVL (Fig. 3) collected from a tall, straight tree with good
canopy cover in a home garden (bordering the forest) in
September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
Fig. 2. Close-ups of Cnemaspis anslemi sp. nov. male holotype
weil »
(NMSL.2019.14.01): (A) dors
f ‘ C wh
> . A
f x
al, (B) lateral, (C) ventral aspects of
head, (D) scales on lateral surface of trunk, (E) smooth ventral scales, (F) homogeneous dorsal scales, (G) cloacal characters with
femoral pores, (H) subdigital lamellae on pes, (I) subdigital lamellae on manus, (J) lateral side of tail, (IK) oval shaped subcaudals,
and (L) dorsal scalation of tail. Photos: Suranjan Karunarathna.
Udamaliboda, Kegalle District, Sabaragamuwa Province,
Sri Lanka (6.859728°N, 80.448736°E, WGS1984;
elevation 485 m, around 14.00 hrs), on 27 March 2019
by Suranjan Karunarathna and Kanishka Ukuwela.
Diagnosis. Cnemaspis anslemi sp. nov. can be readily
distinguished from its Sri Lankan congeners by a
combination of the following morphological and meristic
Amphib. Reptile Conserv.
characteristics, and also color pattern: maximum SVL
34.4 mm; dorsum with homogeneous, smooth granular
scales; 2/2 supranasals, one internasal, and 1/1 postnasal
present; three enlarged postmentals; postmentals
bounded by five chin scales; chin and gular scales
smooth, granular, juxtaposed; pectoral and abdominal
scales smooth and subimbricate; 3—5 well developed
tubercles on posterior flank; 118-122 paravertebral
September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
Fig. 3. Dorsal and ventral aspects of the type series of Cnemaspis anslemi sp. nov. (A) Male holotype, NMSL.2019.14.01, (B) fe-
male paratype, NMSL.2019.14.02, and (C) female paratype, NMSL.2019.14.03 from Udamaliboda, Samanala Nature Reserve, Sri
Lanka. Photos: Suranjan Karunarathna.
granules linearly arranged; 19-21 belly scales across
venter; precloacal pores absent in males, 14—15 femoral
pores on each side in males separated by 9-11 unpored
interfemoral scales in males, and 2—3 unpored posterior
femoral scales in males; 111-117 ventral scales; 87-91
midbody scales; subcaudals smooth, subhexagonal,
enlarged, subequal, forming a regular median row; 8—9
supralabials; 8—9 infralabials; 16-17 total lamellae on
digit IV of manus, and 20—21 total lamellae on digit I'V of
pes (Table 1). Dorsal body reticulated brown, black, and
white; two large oval patches present on the neck; chin
and gular with bright yellow, and femur dirty yellow.
Comparisons with other species. Based on the
presence of enlarged hexagonal subcaudal scales C.
anslemi sp. nov. can be assigned to the C. podihuna
clade sensu Agarwal et al. (2017). However, the new
species may be readily differentiated from congeners in
this clade as follows: from C. kandambyi Batuwita and
Udugampala, 2017, C. molligodai Wickramasinghe and
Munindradasa, 2007, and C. podihuna Deraniyagala,
1944 by absence (versus presence) of precloacal pores;
from C. alwisi Wickramasinghe and Munindradasa,
2007, C. godagedarai de Silva et al. 2019, C. hitihami
Karunarathna et al. 2019, C. kohukumburai Karunarathna
et al. 2019, C. phillipsi Manamendra-Arachchi et al.
2007, C. punctata Manamendra-Arachchi et al. 2007,
C. rajakarunai Wickramasinghe et al. 2016, and C.
rammalensis Vidanapathirana et al. 2014 by the presence
of fewer ventral scales (111-117 versus 145-153, 133-
137, 132-135, 131-134, 128-143, 129-137, 146-186,
and 186—207, respectively); from C. ni/gala Karunarathna
et al. 2019 by the presence of more femoral pores (14—
15 versus 7-9), from C. gemunu Bauer et al. 2007 by
the presence of a greater number of belly scales (19-21
versus 13-16) and by presence of more paravertebral
granules (118—122 versus 79-93); and from C. scalpensis
Amphib. Reptile Conserv.
(Ferguson, 1877) by the presence of fewer tubercles on
posterior flank (3—5 versus 9-11) and a greater number of
paravertebral granules (118-122 versus 102-112).
Among species of the C. kandiana clade sensu
Agarwal et al. (2017), C. anslemi sp. nov. differs by the
absence (versus presence) of precloacal pores and the
presence (versus absence) of clearly enlarged, hexagonal,
or subhexagonal subcaudal scales from the following
species: C. amith Manamendra-Arachchi et al. 2007,
C. butewai Karunarathna et al. 2019, C. gotaimbarai
Karunarathna et al. 2019, C. ingerorum Batuwita et al.
2019, C. kallima Manamendra-Arachchi et al. 2007, C.
kandiana (Kelaart, 1852), C. kivulegedarai Karunarathna
et al. 2019, C. kumarasinghei Wickramasinghe and
Munindradasa, 2007, C. latha Manamendra-Arachchi
et al. 2007, C. menikay Manamendra-Arachchi et al.
2007, C. nandimithrai Karunarathna et al. 2019, C.
pava Manamendra-Arachchi et al. 2007, C. pulchra
Manamendra-Arachchi et al. 2007, C. retigalensis
Wickramasinghe and Munindradasa, 2007, C.
samanalensis Wickramasinghe and Munindradasa,
2007, C. silvula Manamendra-Arachchi et al. 2007,
C. tropidogaster (Boulenger, 1885) and C. upendrai
Manamendra-Arachchi et al. 2007.
Description of Holotype. An adult male, 34.4 mm SVL.
Body slender and relatively long (TRL 42.3% of SVL).
Head relatively large (HL 30.3% of SVL, HL 71.6% of
TRL), narrow (HW 17.2% of SVL, HW 56.7% of HL),
depressed (HD 10.0% of SVL, HD 33.1% of HL) and
distinct from neck. Snout relatively long (ES 80.7% of
HW, ES 45.8% of HL), more than twice the eye diameter
(ED 38.4% of ES), more than half the length of jaw (ES
67.8% of JL), snout slightly concave in lateral view; eye
relatively small (ED 17.6% of HL), twice as large as ear
(EL 34.4% of ED), pupil rounded; orbit length greater
than eye to ear distance (OD 115.6% of EE) and greater
September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
Table 1. Morphometric and meristic data of holotype and paratypes of Cnemaspis anslemi sp. nov. from Udamaliboda, Sri Lanka.
Abbreviations: Holo—holotype, Para—paratype, M—male, F—female, L—left, R-right.
NMSL NMSL NMSL NMSL NMSL NMSL
Measurement 2019.14.01 2019.14.02 2019.14.03 Counts 2019.14.01 2019.14.02 2019.14.03
Holo (M) Para (F) Para (F) Holo (M) Para (F) Para (F)
SVL 34.4 32,3 30.3 FLSP (L/R) 5/5 3/3 4/3
ED 1.8 1.8 1.8 SUP (L/R) 8/8 9/8 8/8
OD 3.3 39 3.1 INF (L/R) 9/8 8/8 8/8
EN 2.9 oo ih INOS 27 ZY 26
ES 4.8 4.7 4.6 PM 3 5 3
SN 1,3 bal 1.1 CHS 5 3 ES
NW ORF OZ 0.2 SUN (L/R) 2/2 2/2 2/2
EE 29 De Df PON (L/R) 1/1 1/1 1/1
SA 16.9 LS 15<2 INT 1 1 1
EL 0.6 0.6 0.6 SUS (L/R) 9/10 11/11 10/9
IO 3.4 aS 3:3 BET (L/R) 18/18 18/17 19/18
IE 4.8 4.7 4.7 CAS (L/R) 9/10 8/8 9/8
HL 10.4 99 a9 TLM (i) (L/R) 11/11 10/11 10/10
HW 59 5.8 ae TLM (ii) (L/R) 12/12 12/13 12/11
HD 3.5 Br 3.0 TLM (iit) (L/R) 14/13 14/14 13/13
JL 7.0 6.9 6.9 TLM (iv) (L/R) 17/17 17/16 17/17
IN 1.7 1.8 1.7 TLM (v) (L/R) 13/13 13/13 13/12
SED 95 9.4 9.4 PG | ese 118 121
UAL 5.1 4.9 49 MBS 87 91 90
LAL ras 3.l 5.1 MVS 117 112 111
PAL 4.6 D7 +9 BLS 21 19 19
DLM (1) 1.4 1.3 1.4 TLP (i) (L/R) 9/9 9/9 9/9
DLM (11) 2.8 Dey Deh TLP (ii) (L/R) 13/12 ID 12/13
DLM (111) | 2.9 2D TLP (iti) (L/R) 18/18 19/18 17/18
DLM (iv) 3.3 3:1 3.2 TLP (iv) (L/R) 21/21 21/20 21/21
DLM (v) 2 2.4 2.4 TLP (v) (L/R) 16/16 15/16 15/15
TRL 14.6 23 12.0 FP (L/R) 15/14 - -
TW 6.3 6.1 6.2 PFS (L/R) 3/2 - -
TD 3.8 39 a IFS 10 - -
PEL Fel 6.9 69
TBL 6.2 6.1 6.1
HEL 6.2 6.3 672
DLP (1) 22, | ow)
DLP (11) 3.4 3:2 3.4
DLP (111) 3.8 3.8 3.7
DLP (iv) 4.2 4] 4.2
DLP (v) 3.6 35 3.6
TAL 39.4 36.5 34.7
TBW 3.8 3,5 3.4
TBD 3.1 vA, Sie
than the length of digit IV of the manus (OD 100.3% of
DLM IV); supraocular ridges not prominent; ear opening
very small (EL 6.0% of HL), deep, taller than wide, larger
than nostrils; single row of scales separates orbit from
supralabials; interorbital distance is narrow (IO 72.1% of
ES), shorter than head length (IO 33.0% of HL); eye to
Amphib. Reptile Conserv.
nostril distance slightly greater than eye to ear distance
(EN 102.1% of EE).
Dorsal surface of the trunk with smooth, small
homogeneous granules, 122 paravertebral granules;
117 smooth midventral scales; 87 midbody scales; 5/5
well developed tubercles on flanks; ventrolateral scales
September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
slightly enlarged; granules on snout smooth and flattened,
larger than those on interorbital and occipital regions;
canthus rostralis not pronounced, 9/10 smooth oval
scales from eye to nostril; scales of interorbital region
oval and smooth; 2/2 weakly developed tubercles present
on sides of neck and around ear; ear opening vertically
oval, slanting from anterodorsal to posteroventral, 18/18
scales between anterior margin of the ear opening and
posterior margin of eye. Supralabials 8/8 and infralabials
9/8, becoming smaller towards the gape. Rostral scale
wider than long, partially divided (90%) by a median
groove and in contact with first supralabial. Nostrils
separated by 2/2 enlarged supranasals with one internasal
and 1/1 postnasal; no enlarged scales behind supranasals.
Nostrils oval, dorsolaterally oriented, not in contact with
first supralabials.
Mental subrhomboidal, as wide as long, posteriorly
in contact with three enlarged postmentals (smaller
than mental, and larger than chin scales); postmentals
in contact and bordered posteriorly by five smooth chin
scales (larger than nostrils), contact with the 1‘ and 2"4
infralabials; ventral scales smaller than chin scales,
and larger than nostrils. Smooth, rounded, juxtaposed
granule-like scales on chin and gular region; pectoral
and abdominal scales smooth, subimbricate towards
precloacal region, abdominal scales larger than dorsals;
21 belly scales across venter; smooth, subimbricate scales
around vent and base of tail; 15/14 femoral pores; 10
unpored interfemoral scales; 3/2 small posterior femoral
scales. Original tail of holotype longer than snout-vent
length (TAL 114.5% of SVL); hemipenial bulge greatly
swollen (TBW 3.8 mm), homogeneous scales on dorsal
aspect of tail directed posteriorly, 1/1 spine-like tubercles
present at base of tail, subcaudals very smooth; tail with
3-4 enlarged flattened obtuse scales forming whorls;
absence of post-cloacal spur on each side; smooth
subcaudals arranged into a median series of clearly
enlarged, hexagonal or subhexagonal scales.
Forelimbs moderately short, slender (LAL 15.1%
of SVL, UAL 14.8% of SVL) lower arm longer than
upper arm; hind limbs moderately long, tibia shorter
than femur (TBL 18.1% of SVL, FEL 20.5% of SVL).
Dorsal, anterior, ventral, and posterior surfaces of upper
arm with smooth scales, those on anterior surface twice
as large as those on other faces of limb; dorsal, anterior,
ventral, and posterior surfaces of lower arm with smooth
scales, those on posterior surface twice as large as
those of other parts; scales on dorsal surface of femur
smooth and granular, less imbricate scales on anterior,
posterior and ventral surfaces, scales on anterior surface
are twice the size of those of other aspects. All surfaces
of tibia with smooth scales; both anterior and posterior
surfaces of limbs bearing smooth granules, scales of the
ventral surface twice as large as those of other aspects.
Dorsal and ventral scales on the manus and the pes
smooth, granular; dorsal surfaces of digits with granular
scales. Digits elongate and slender with inflected distal
Amphib. Reptile Conserv.
phalanges, all bearing slightly recurved claws. Subdigital
lamellae entire (except divided at first interphalangial
joint), unnotched; total lamellae on manus (left/right):
digit I (11/11), digit IT (12/12), digit III (14/13), digit
IV (17/17), digit V (13/13); total lamellae on pes (left/
right): digit 1 (9/9), digit (13/12), digit IM (18/18), digit
IV (21/21), digit V (16/16); interdigital webbing absent;
length order of digits of manus (left): I (1.4 mm), V (2.5
mm), II (2.8 mm), II (3.1 mm), IV (3.3 mm); length
order of digits of pes (left): I (2.2 mm), II (3.4 mm), V
(3.6 mm), II (3.8 mm), IV (4.2 mm).
Variation of the type series. The SVL of adult speci-
mens in the type series (n = 3) and others (n = 5) ranges
from 30.3 to 34.4 mm, TAL ranges from 34.7—39.4 mm,
and TRL ranges from 12.0—14.6 mm; number of supral-
abials 8—9, and infralabials 8—9 (Table 1); spines on flank
3-5; interorbital scales 26—29; supraciliaries 9-11; can-
thal scales 8-10; scales from eye to tympanum 17-19;
total lamellae on digits of manus: digit I (10-11), digit
II (11-13), digit I (13-14), digit ITV (16-17), digit V
(12-13); total lamellae on digits of pes: digit I (12-13),
digit HI (17-19), digit [V (20-21), digit V (15-16); ven-
tral scales 111-117, midbody scales 87-91; paravertebral
granules 118—122; belly scales 19-21; unpored interfem-
oral scales 9-11 in males; femoral pores in males 14—15,
and unpored posterior femoral scales in males 2-3.
Color of living specimens. The body color on the dorsal
side is reddish brown; the dorsal head is randomly
scattered with black and white dots; a yellowish oval
patch on occiput, and a straight black middorsal dash
over midpoint of neck (Fig. 4); faded yellow patches
along vertebral midline; indistinct dark canthal stripe
extends through eye and above ear, terminating anterior
to forelimb insertion; the pupil of eye is circular and
black with the surrounding being golden brown; a series
of 4-5 mottled, irregular, dark brown transverse bands
with gray margins on dorsum of body; dorsum of tail
with 13—15 cinnamon brown blotches separating 12-14
faded dark brown bands; lateral view of labials and neck
consists of thin black dots in bright yellow background
like a zigzag mark; small dark spots (like eyes) present
on back side of femur; chin and gular with bright yellow,
vent and femur completely dirty yellow color.
Color of preserved specimens. Dorsum is light brown;
dorsum of head is randomly scattered with brown and
cream dots; an oval cream color patch on occiput, and
a straight dark brown middorsal dash over midpoint of
neck; a white post-orbital stripe present; labials with
black and cream spots; venter is completely dirty white;
tail with scattered markings on dorsal side.
Etymology. The specific epithet is an eponym Latinized
(anslemi) in the masculine genitive singular, honoring
the veteran Sri Lankan herpetologist Kongahage Anslem
September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
me i Fe oa See bd :
Fig. 4. Cnemaspis anslemi sp. nov. male holotype
(NMSL.2019.14.01) in life in-situ. (A) Dorsal view of the full
body displaying the typical color pattern and a straight black
middorsal dash over midpoint of neck, (B) Ventral aspect show-
ing gular and femoral colorations, (C) lateral view showing la-
bial coloration and zigzag pattern, (D) dorsal view of the full
body of female paratype (NMSL.2019.14.02) in life in-situ
from Udamaliboda, Samanala Nature Reserve, Sri Lanka. Pho-
tos: Kanishka Ukuwela and Suranjan Karunarathna.
Lawrence de Silva (the father of modern herpetology in
Sri Lanka) for his valuable contributions to Sri Lankan
herpetology and for inspiring the next generation of
herpetologists, including the authors.
Natural history. The lower Samanala Nature Reserve
area (along with Udamaliboda) comprises home gardens,
and tropical evergreen rainforests (Gunatileke and Guna-
tileke 1990) mixed with tea and rubber plantations. The
area comprises the Ratnapura and Kegalle districts and
lies between 6.759172° and 6.889842°N and 80.436194°
and 80.487717°E, at an elevation of 350-850 m. The
mean annual rainfall varies between 3,500 and 4,500
mm, received mostly via the southwest monsoon (May—
September). The mean annual temperature of the area
is 26.4—27.9 °C. Cnemaspis anslemi sp. nov. 1s a quite
rare species as six (+ 0.1) geckos per survey-hour were
found after covering a total area of 20 ha. This species
was restricted to tall straight trees with smooth bark and
thick canopy cover, and houses with tall clay walls with
crevices. These geckos could climb up to 7 m on vertical
surfaces of trees (Fig. 5). They were active during the day
Amphib. Reptile Conserv.
21
ees :
oki ae
maliboda, Samanala Nature Reserve, Kegalle District, Sri Lan-
ka. (A) Complete view of the forest hill, (B) shady forest with
thick leaf litter, (C) hundred years old house made using clay
and bricks, also with wattle and daub, (D) communal egg lay-
ing site on a clay wall. Photos: Madhava Botejue and Suranjan
Karunarathna.
time (08.00—17.00 h) and, when disturbed, sought ref-
uge in tree tops with crevices. The new species was sym-
patric (at local habitat scale) with several other geckos
(Cnemaspis samanalensis, Cnemaspis sp., Cyrtodactylus
triedrus, Cyrtodactylus sp., Gehyra mutilata, Hemidac-
tylus depressus, H. pieresii, H. frenatus, H. parvimacula-
tus, and Hemiphyllodactylus typus). The eggs were pure
white in color and almost spherical in shape (~5 mm),
with a slightly flattened side that attached to the clay-wall
substrate. This species has also been recorded from the
Lihinihela, Borangamuwa, and Warnagala areas in lower
Samanala Nature Reserve.
Conservation status. Application of the IUCN Red List
criteria indicates that C. anslemi sp. nov. is Critically
Endangered (CR) due to having an area of occupancy
(AOO) < 10 km? (six locations, 0.2 km? in total, assum-
ing a 100 m radius around the georeferenced locations)
and an extent of occurrence (EOO) < 100 km? (96.7 km?)
in the lower elevations of Central Province [Applicable
criteria are B2-b (i11)].
Remarks. Cnemaspis anslemi sp. nov. most closely
resembles C. gemunu, C. godagedarai, C. phillipsi, and
C. scalpensis. The type localities of these species are
September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
Table 2. Key characters and identification features of 12 species belonging to the podihuna clade (scalpensis group), Sri Lanka. For
these species, the dorsal scales are homogeneous, ventral scales are smooth, and subcaudal scales are clearly enlarged, hexagonal,
or subhexagonal. Abbreviations: SVL—maximum snout to vent length in mm; SUP-supralabials; INF—infralabials; VEN—ventral
scales; BEL—belly scales; FSP—spines on the flank; MBO-midbody scales; PVT—paravertebral scales; UPF—unpored interfemoral
scales; FEP—femoral pores; LF4—lamellae on 4" finger; and LT4—lamellae on 4" toe.
FSP MBO PVT UPF FEP LF4 LT4
4-5 71-78 89-97 18-19 7-9 15-17-1721
3-4 87-9] 118-122 9-11 14-15 16-17 20-21
7-8 74-87 79-93 10-12 11-14 =15-17—- 18-19
5-6 98-102 101-106 8-9 12-13. 17-18 20-21
4-5 96-99 143-149 24-26 5-10 18-19 21-22
7-8 81-88 150-159 24-25 6-9 21-22 23-25
3-4 71-78 179-187 14-15 7-9 17-18 17-18
4-6 76-91 86-93 11-14 15-16 16-19 17-19
11-13 71-78 83-91 25-27 5-7 17-18 17-23
5-6 69-74 81-85 20-22 7-8 16-20 19-22
4-5 119-131 94-96 19-24 14-16 22-23 22-23
9-11 81-89 102-112 8-12 13-15 17-18 19-21
Species SVL SUP INF VEN BEL
C. alwisi 40.4 8-10 7-9 145-153 27-31
C. anslemi 34.4 8-9 8-9 111-117 19-21
C. gemunu 34.0 8-10 7-8 112-118 =13-16
C. godagedarai 35.5 7-8 7-8 133-137. 21-23
C. hitihami 41.7 8-9 7-9 132-135 21-22
C. kohukumburai 34.5 8-9 7-8 131-134 22-23
C. nilgala 32.9 7-8 6-7 122-129 17-19
C. phillipsi 36.6 8-9 8-9 128-143 =: 18-25
C. punctata 39.9 7-10 7-9 129-137 20-29
C. rajakarunai 40.2 8-9 9-1] 146-186 26-29
C. rammalensis 53.8 8-10 8-9 186-207 25-28
C. scalpensis 36.6 7-9 7-8 120-131 17-19
separated by ~38 km (Haggala in Nuwara Eliya), ~55
km (Ensalwatte in Deniyaya), ~83 km (Gammaduwa
in Matale), and ~47 km (Gannoruwa in Kandy) airline
distances, respectively, from Udamaliboda in Kegalle
(Fig. 1). Further, the new species can be distinguished
from C. gemunu, C. godagedarai, C. phillipsi, and C.
scalpensis by morphometric and meristic characters
(Table 2). We believe Cnemaspis cf. gemunu (AMB
7507, now in NMSL) collected from Borangamuwa in
Ratnapura District (6.742778°N, 80.707778°E; elevation
about 800 m) would most likely represent C. anslemi sp.
nov. according to the currently known distribution pattern
(see Agarwal et al. 2017). The records of Cnemaspis
scalpensis from Udamaliboda forest and vicinity by
Peabotuwage et al. (2012) also represent Cnemaspis
anslemi sp. nov.
Discussion
The discovery and description of a novel species here
adds yet another member to this speciose genus, increas-
ing the known diversity of Cnemaspis in Sri Lanka to 33
species, all of which are endemic to the island. Several
new descriptions during the last decade (e.g., Bauer et
al. 2007; Manamendra-Arachchi et al. 2007; Wickrama-
singhe and Munindradasa 2007; Vidanapathirana et al.
2014; Wickramasinghe et al. 2016; Batuwita and Udu-
gampala 2017; Batuwita et al. 2019; de Silva et al. 2019;
Karunarathna et al. 2019a,b) have greatly advanced our
knowledge on the diversity of these diminutive day geck-
Os, Increasing the total diversity from just four species.
This trend most likely suggests that the diversity of Sri
Lankan Cnemaspis is still underestimated, and further
studies would most likely reveal more species from the
varied natural and semi-natural habitats of Sri Lanka.
Although Sri Lankan Cnemaspis are likely derived from
the Indian radiation, the current diversity of this genus 1s
Amphib. Reptile Conserv.
probably the result of multiple colonization events (poly-
phyletic origin) as opposed to a single in situ radiation
(monophyly); however, these phylogenetic and biogeo-
graphic affinities have yet to be confirmed (Agarwal et
al. 2017; Bauer et al. 2007; Karunarathna et al. 2019b).
We tentatively assign this species to the podihuna clade
on the basis of clearly enlarged, hexagonal, or subhex-
agonal subcaudal scales (Fig. 6).
The preliminary studies reported here indicate that
this novel species is frequently found in home garden
habitats, as opposed to natural forest habitats, in the
Udamaliboda region (Samanala Nature Reserve). Dur-
ing the survey from 2006 to 2019, only five specimens
were found in the natural forest habitats of the Samanala
Nature Reserve. The home gardens in which the new
Species was observed are heavily shaded and humid. The
low encounter rates in natural forests could also be due to
the low visibility conditions caused by the dense canopy,
and this species may possibly occupy higher perches on
the tree trunks, thus avoiding detection. However, fur-
ther studies are necessary to ascertain this fact. Like most
of the Sri Lankan Cnemaspis known so far (Bauer et al.
2007; Agarwal et al. 2017), the new species has a very
small range, most likely due to the narrow ecological
niche of this species (Slatyer et al. 2013). Its small size
may reduce both dispersal ability as well as ecological
tolerance levels. The Udamaliboda trail of Samanala Na-
ture Reserve 1s inhabited by 11 species of geckos, includ-
ing two undescribed species, two Critically Endangered,
two Endangered, and two Vulnerable species (Peabotu-
wage et al. 2012). Overall, 65 reptile species have already
being recorded from the type locality, indicating that the
Udamaliboda 1s a local hotspot of reptile diversity.
The type locality of this species and the surrounding
areas are currently subjected to encroachment via tea cul-
tivation and mini-hydropower projects. Such activities
will certainly reduce the crucial natural and semi-natural
September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
Fig. 6. Morphological characters that differentiate the species of podihuna and kandiana clades. (A) Scales and pores around vent
in podihuna clade, (B) scales and pores around vent in kandiana clade, (C) keeled and imbricate belly scales, (D) smooth and imbri-
cate belly scales, (E) heterogeneous keeled dorsal granules, (F) homogeneous smooth dorsal granules, (G) smooth sub-hexagonal
subcaudals in podihuna clade, (H) smooth, solid hexagonal subcaudals in podihuna clade, (1) smooth, small, and irregular subcau-
dals in kandiana clade, (J) keeled, small, and irregular subcaudals in kandiana clade (yellow arrows: unpored posterior femoral
scales in males; blue arrows: femoral pores in males; green arrows: unpored anterior femoral scales in males; red arrows: precloacal
pores in males; white arrows: unpored interfemoral scales in males).
habitats of this range-restricted species. Thus, authorities rare or even undescribed species is minimized.
should carefully consider new proposals for mini-hydro-
power plants near or within natural habitats like these,in Acknowledgements.—We thank Chandana Sooriyaban-
order to ensure that loss of the habitats occupied by such _—_ dara (The Director General of DWC), Laxman Peiris
Amphib. Reptile Conserv. 23 September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
(Deputy Director — Research division of DWC), the re-
search committee, and the field staff of the Department
of Wildlife (WL/3/2/1/14/12 and WL/3/2/42/18 a and b)
and Conservator General of Forest Department (FRC/5,
and FRC/6) for granting permission and the field staff
for assisting during the field surveys. Nanda Wickrama-
singhe, Sanuja Kasthuriarachchi, Lankani Somaratne,
Chandrika Munasinghe, Rasika Dasanayake, Ravindra
Wickramanayake, and P. Gunasiri at NMSL assisted
while we were examining collections under their care.
Anslem de Silva, Aaron Bauer, Thilina Surasinghe, Bud-
dhika Madurapperuma, Chamara Amarasinghe, Tharaka
Kusuminda, Indika Peabotuwage, Nirmala Perera, Mad-
hava Botejue, Dinesh Gabadage, Hasantha Wiyethunga,
D.M. Karunarathna, Kawmini Karunarathna, Rashmini
Karunarathna, Thesanya Karunarathna, and Niranjan
Karunarathna provided valuable assistance in numerous
stages of this study. This work was mainly supported by a
Nagao Natural Environment Foundation (2018-20) grant
to SK. Finally, we would like to thank the anonymous
reviewers for constructive comments that helped to im-
prove the manuscript.
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Suranjan Karunarathna obtained his Masters in Environmental Management at the University
of Colombo, Sri Lanka. His scientific exploration of biodiversity began with the Young Zoologists’
Association of Sri Lanka (YZA) in early 2000, and he served as president of YZA in 2007. As a
wildlife researcher, Suranjan conducts research on herpetofaunal ecology and taxonomy, and he
also promotes the scientific basis for raising awareness on the importance of biodiversity and its
conservation among the Sri Lankan community. He is an active member of many specialist groups
in the IUCN/SSC, and an expert committee member for herpetofauna in the National Red List
development programs, Sri Lanka, since 2004. Photo: Lark Hayes.
Kanishka D.B. Ukuwela is currently a Senior Lecturer in Zoology at the Rajarata University
of Sri Lanka. He holds a B.S. (Hons.) degree in Zoology from the University of Peradeniya, Sri
Lanka and a Ph.D. in Evolutionary Biology from the University of Adelaide, Australia. His current
research is focused on the origins, evolution, systematics, and conservation of the South Asian
herpetofauna. Photo: [suri Jayawardena.
September 2019 | Volume 13 | Number 2 | e187
New species of Cnemaspis from Sri Lanka
Appendix 1.
Comparative material:
Cnemaspis alwisi. NMSL 2004.09.01 (holotype), NMSL 2004.09.02 (paratype), NMSL 2004.09.03 (paratype), WHT
5918, WHT 6518, WHT 6519, WHT 7336, WHT 7337, WHT 7338, WHT 7343, WHT 7344, WHT 7345, WHT 7346.
C. amith: BMNH 63.3.19.1066A (holotype), BMNH 63.3.19.1066B (paratype), BMNH 63.3.19.1066C (paratype).
C. butewai: NMSL 2019.07.01 (holotype), NMSL 2019.07.02 (paratype), NMSL 2019.07.03 (paratype).
C. gemunu: AMB 7495 (holotype), AMB 7507 (paratype?), WHT 7221, WHT 7347, WHT 7348, NMSL 2006.11.01,
NMSL 2006.11.02, NMSL 2006.11.03, NMSL 2006.11.04.
C. godagedarai: NMSL 2019.09.01 (holotype), NMSL 2019.16.01 (paratype), NMSL 2019.16.02 (paratype).
C. gotaimbarai: NMSL 2019.04.01 (holotype), NMSL 2019.04.02 (paratype), NMSL 2019.04.03 (paratype).
C. hitihami. NMSL 2019.06.01 (holotype), NMSL 2019.06.02 (paratype), NMSL 2019.06.03 (paratype).
C. ingerorum. WHT 7332 (holotype), WHT 7330 (paratype), WHT 7331 (paratype).
C. kallima: WHT 7245 (holotype), WHT 7222 (paratype), WHT 7227 (paratype), WHT 7228 (paratype), WHT 7229
(paratype), WHT 7230(paratype), WHT 7239 (paratype), WHT 7249 (paratype), WHT 7251 (paratype), WHT 7252
(paratype), WHT 7253 (paratype), WHT 7254 (paratype), WHT 7255 (paratype).
C. kandambyi. WHT 9466 (holotype), WHT 9467 (paratype).
C. kandiana: BMNH 53.4.1.1 (lectotype), BMNH 80.2.2.119A (paralectotype), BMNH 80.2.2.119B (paralectotype),
BMNH 80.2.2.119C (paralectotype), WHT 7212, WHT 7213, WHT 7267, WHT 7305, WHT 7307, WHT 7308, WHT
7310, WHT 7313, WHT 7319, WHT 7322.
C. kivulegedarai: NMSL 2019.08.01 (holotype), NMSL 2019.08.02 (paratype), NMSL 2019.08.03 (paratype).
C. kohukumburai: NMSL 2019.05.01 (holotype), NMSL 2019.05.02 (paratype), NMSL 2019.05.03 (paratype).
C. kumarasinghei: NMSL 2006.13.01 (holotype), NMSL 2006.13.02 (paratype).
C. latha: WHT 7214 (holotype).
C. menikay: WHT 7219 (holotype), WHT 7218 (paratype), WHT 7349 (paratype).
C. molligodai: NMSL 2006.14.01 (holotype), NMSL 2006.14.02 (paratype), NMSL 2006.14.03 (paratype), NMSL
2006.14.04 (paratype), NMSL 2006.14.05 (paratype).
C. nandimithrai: NMSL 2019.01.01 (holotype), NMSL 2019.01.02 (paratype), NMSL 2019.01.03 (paratype).
C. nilgala: NMSL 2018.07.01 (holotype), NMSL 2018.06.01 (paratype), NMSL 2018.06.02 (paratype), NMSL
2018.06.03 (paratype).
C. pava: WHT 7286 (holotype), WHT 7281 (paratype), WHT 7282 (paratype), WHT 7283 (paratype), WHT 7285
(paratype), WHT 7288 (paratype), WHT 7289 (paratype), WHT 7290 (paratype), WHT 7291 (paratype), WHT 7292
(paratype), WHT 7293 (paratype), WHT 7294 (paratype), WHT 7295 (paratype), WHT 7296 (paratype), WHT 7297
(paratype), WHT 7298 (paratype), WHT 7299 (paratype), WHT 7300 (paratype), WHT 7301 (paratype), WHT 7302
(paratype).
C. phillipsi. WHT 7248 (holotype), WHT 7236 (paratype), WHT 7237 (paratype), WHT 7238 (paratype).
Amphib. Reptile Conserv. 26 September 2019 | Volume 13 | Number 2 | e187
Karunarathna and Ukuwela
C. podihuna. BMNH 1946.8.1.20 (holotype), NMSL 2006.10.02, NMSL 2006.10.03, NMSL 2006.10.04.
C. pulchra: WHT 7023 (holotype), WHT 1573a (paratype), WHT 7011 (paratype), WHT 7021 (paratype), WHT 7022
(paratype).
C. punctata. WHT 7256 (holotype), WHT 7223 (paratype), WHT 7226 (paratype), WHT 7243 (paratype), WHT 7244
(paratype).
C. rajakarunai: NMSL 2016.07.01 (holotype), DWC 2016.05.01 (paratype), DWC 2016.05.02 (paratype).
C. rammalensis: NMSL 2013.25.01 (holotype), DWC 2013.05.001.
C. retigalensis: NMSL 2006.12.01 (holotype), NMSL 2006.12.02 (paratype), NMSL 2006.12.03 (paratype), NMSL
2006.12.04 (paratype).
C. samanalensis: NMSL 2006.15.01 (holotype), NMSL 2006.15.02 (paratype), NMSL 2006.15.03 (paratype), NMSL
2006.15.04 (paratype), NMSL 2006.15.05 (paratype).
C. scalpensis: NMSL 2004.01.01 (neotype), NMSL 2004.02.01, NMSL 2004.03.01, NMSL 2004.04.01, WHT 7265,
WHT 7268, WHT 7269, WHT 7274, WHT 7275, WHT 7276, WHT 7320.
C. silvula: WHT 7208 (holotype), WHT 7206 (paratype), WHT 7207 (paratype), WHT 7209 (paratype), WHT 7210
(paratype), WHT 7216 (paratype), WHT 7217 (paratype), WHT 7018, WHT 7027, WHT 7202, WHT 7203, WHT
7220, WHT 7354, WHT 7333.
C. tropidogater. BMNH 71.12.14.49 (lectotype), NMSL 5152, NMSL 5151, NMSL 5159, NMSL 5157, NMSL 5970,
NMSL 5974.
C. upendrai: WHT 7189 (holotype), WHT 7184 (paratype), WHT 7187 (paratype), WHT 7188 (paratype), WHT 7181
(paratype), WHT 7182 (paratype), WHT 7183 (paratype), WHT 7185 (paratype), WHT 7190 (paratype), WHT 7191
(paratype), WHT 7192 (paratype), WHT 7193 (paratype), WHT 7194 (paratype), WHT 7195 (paratype), WHT 7196
(paratype), WHT 7197 (paratype), WHT 7260 (paratype).
Amphib. Reptile Conserv. 27 September 2019 | Volume 13 | Number 2 | e187
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 28-30 (e188).
Book Review
How Snakes Work: Structure, Function
and Behavior of the World’s Snakes
Brian I. Crother
Department of Biological Sciences, Southeastern Louisiana University, Hammond, Louisiana, USA
Keywords. Reptilia, Squamata, Ophidia, anatomy, locomotion, physiology, reproduction, thermoregulation
Citation: Crother BI. 2019. Book Review—How Snakes Work: Structure, Function and Behavior of the World’s Snakes. Amphibian & Reptile
Conservation 13(2) [General Section]: 28—30 (e188).
Copyright: © 2019 Crother. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 In-
ternational (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows:
Official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 26 August 2019; Accepted: 29 August 2019; Published: 12 September 2019
“They are magnificent. They are splendid creations
ingeniously constructed after eons of gradual
change.” Kauffeld, Snakes and Snake Hunting, 1957
There are many books about snakes for every level of
understanding, but rarely, if ever, has there been a book
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As I went through the volume, I kept thinking how I wish
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the reasons why snake are magnificent organisms.
The volume is in a comfortable 8 1/2 by 11-inch
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the end of each chapter. Rick Shine wrote the Foreword
and Lillywhite explains in a short Preface his personal
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“might bring a unique perspective to the subject matter,
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in reaching those goals. Perhaps the reason he is so
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expertise and passion with us in such a volume.
There are nine chapters: 1) Evolutionary History and
Classification, 2) Feeding, Digestion, and Water Balance,
3) Locomotion: How Snakes Move, 4) Temperature
Correspondence. bcrother@southeastern.edu
Amphib. Reptile Conserv.
and Ectothermy, 5) Structure and Function of Skin,
6) Internal Transport: Circulation and Respiration,
7) Perceiving the Snake’s World: Structure and
Function of Sense Organs, 8) Sound Production, and 9)
Courtship and Reproduction. There is obviously a lot of
information here and it is as up to date as it could be.
Each of the chapters is wonderfully adorned with terrific
photos and illustrations that help the reader grasp and/or
visualize the text descriptions.
Even in a book on how snakes work, a chapter on
evolution and classification is practically obligatory
because it puts the rest of the book’s information into
context. Maybe the most important nugget of knowledge
given in this chapter is “The latter [snakes] are essentially
highly derived lizards.” It is critical to point out that
snakes are not related to lizards, but are lizards. That
realization makes all the novel evolutionary changes
relative to lizards that are described in this book even
more remarkable. With that fact written in the book, it
is somewhat unfortunate that an accompanying figure
shows snakes and lizards as separate branches on a
phylogeny of the tetrapods. The natural history comments
in the “tip toe through the taxa” section of the chapter are
a welcome addition.
An example of how having a volume written by a
professional research scientist enhances the content
is near the beginning of Chapter 2. Lillywhite wrote,
“The following discussion 1s essentially speculative,
but it provides a conceptual basis from which to launch
considerations of feeding and digestion in snakes.”
Because of his long history of work in the field, his
speculations are valuable and make you feel like you
just asked an expert a question and he is giving you
September 2019 | Volume 13 | Number 2 | e188
Crother
his unique insight. I consider it a bonus. Beyond the
speculation, this chapter 1s a trove of information on the
diversity of feeding adaptations among snakes, such as
the physiology required to handle digestion of various
food types, and the myriad aspects of how snakes
physiologically deal with water.
So, you think you know how snakes move? In my
high school term paper that I previously mentioned, I
described three modes: lateral, concertina, and rectilinear
motion. I was woefully incomplete. The illustrations in
Harvey’s book, from anatomy to movement, are excellent
and useful. The final section of this chapter, titled Snakes
as Robots, is a treat.
Of course, we recognize snakes as ectotherms, but
as Lillywhite reveals in Chapter 4 on “Temperature
and Ectothermy,” being an ectotherm is an extremely
complicated deal for snakes. The chapter goes through
these many complications and even provides examples
of endothermy in snakes, which makes the label
“ectotherm” require an even more broad interpretation.
Lillywhite does a great job pointing out how much is not
known about thermoregulation, especially with regard
to trade-offs or cost-benefits when thermoregulation is
coupled with any of the myriad of other physiological
processes of the organism.
There is something magical about seeing snake skin
that is either as glossy as glass, like mud snakes (Farancia
abacura), or spectacularly iridescent, like rainbow boas
(Epicrates cenchria). Well the chapter on skin covers it
all and tells you everything you need (or wanted) to know
about snake skin, from cultural references to histology
and micrographs to mimicry and color/pattern variation.
As usual for this book, the photos and illustrations are
terrific!
The concluding paragraph of the chapter on Internal
Transport opens with: “Few persons probably give
much thought to how the blood circulates within a snake
and how the lung functions to assist in the delivery of
oxygen.” I have to agree with Lillywhite here, but I also
have to add that after reading the chapter one can’t help
but learn things, even if you think you already know
everything there is to know about circulation and gas
exchange in snakes.
One of the most amazing aspects of snake biology
is the way they perceive the environment around them.
Snakes are famous for their chemosensory abilities, and
some groups of snakes are well-known for their thermal
and infrared radiation detection abilities. The chapter
on how snakes perceive the world covers those topics
in excellent fashion. Even though hearing is less of an
obvious pathway for snakes in sensing the environment,
the coverage on that is well done here too. When I teach
herpetology, I love to talk about snake eyes because of all
the novel structures (and of the typical structures that are
absent), because it seems fairly well-established that in
the evolution of snakes the eyes were radically reduced if
not essentially lost.
Amphib. Reptile Conserv.
STRUCTURE, FUNCTION
and BEHAVIOR of the
WORLD'S SNAKES
Title: How Snakes Work: Structure, Function and Behavior
of the World’s Snakes
Author: Harvey B. Lillywhite
Copyright: 2014
ISBN: 978-0-19-538037-8
Publisher: Oxford University Press
Pages: xiii + 241; Price: $61 (USD)
Thus, I was disappointed to see that all those
interesting things were not pointed out in the discussion
of snake eyes in the book. The illustration of the eye
was simplistic and sort of generic. For example, there
are no muscles associated with the ciliary body in snake
eyes, and the conus, sphincter, and dilatator all have
mesodermal origins in snakes, but are ectodermal (!) in
lizards. Those are big differences.
Snake vision received the same generic treatment. For
example, regarding pupil shape, while it's true that a slit
pupil can close more completely than a round pupil, which
the author attributes to crepuscular and nocturnal activity,
that's not the primary function. There are lots of diurnal
snakes with slit pupils. The real function 1s that all animals
with a slit pupil also have a multifocal lens. The slit allows
a reduction in light while still allowing all of that light to
pass through all peripheral layers of the lens (which have
different refractive indices or color filters), rather than just
through the lens center. No doubt, almost every aspect
of snake vision is poorly known, but what is known is
spectacular and its coverage in greater detail would have
fit perfectly well with the rest of this excellent book.
September 2019 | Volume 13 | Number 2 | e188
Book Review: How Snakes Work
When people think of snakes, how many first
think of sound production? Perhaps folks who mainly
encounter rattlesnakes during their lives may associate
snakes with sounds, but typically snakes are associated
with their stealth, with their silence. And that is what
makes the chapter on sound so enjoyable. I want to
hear a gopher snake bellow! I want to hear a cloacal
pop or a king cobra growl! Like vision, there is much
that is not known about snake sound production and
communication, and the author does a nice job bringing
up those questions.
The beginning and end of lineages is intimately tied
to successful reproduction, and the book closes with
a chapter on the subject. It is another very well-done
Amphib. Reptile Conserv.
chapter, with cultural and biological information as well
as bits of expert-based speculation included. I greatly
suspect that for many non-experts this chapter will hold
a number of surprises about snakes, which really, in a
nutshell, is what is great about this book. I very much
like the encouraging, upbeat style of writing that gets the
reader excited about the topics.
I think this is a terrific book for readers with a variety
of knowledge levels. I really believe elementary school
aged kids can get excited by this book and grow with the
book, appreciating it more and more as they learn and
progress through school. I also think the book fits well at
the university level and would be a welcome addition to
any biologist’s library, including herpetologists!
Brian I. Crother is the Schlieder Foundation Professor of Biological Sciences
and interim Department Head of Computer Sciences at Southeastern Louisiana
University in Hammond, Louisiana, USA. Brian earned his B.S. from California
State University at Dominguez Hills, his Ph.D. from the University of Miami,
Florida, USA, and he conducted post-doctoral research at the University of
Texas, Austin. He has well over 100 publications on a broad range of topics,
including edited books on Caribbean Amphibians and Reptiles, Ecology and
Evolution in the Tropics: A Herpetological Perspective and Assumptions that
Inhibit Progress in Comparative Biology. Brian was the chair and coauthor
of the 5" through 8" editions of the Scientific and Standard English Names of
Amphibians and Reptiles of North America North of Mexico. He is active in
several professional organizations and is an ex-president of both the Society for
the Study of Amphibians and Reptiles and the American Society of Ichthyologists
and Herpetologists. Brian’s research interests are broad, but have in common
that they cover amphibians, reptiles, and/or evolution (empirical, theoretical,
and philosophical).
September 2019 | Volume 13 | Number 2 | e188
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 31-94 (e189).
The herpetofauna of Coahuila, Mexico: composition,
distribution, and conservation status
‘David Lazcano, ‘Manuel Nevarez-de los Reyes, *Eli Garcia-Padilla, "Jerry D. Johnson,
3Vicente Mata-Silva, 7Dominic L. DeSantis, and *°*Larry David Wilson
‘Universidad Autonoma de Nuevo Leon, Facultad de Ciencias Biolégicas, Laboratorio de Herpetologia, Apartado Postal 157, San Nicolas de los
Garza, Nuevo Leon, C.P. 66450, MEXICO ?Oaxaca de Juarez, Oaxaca 68023, MEXICO *Department of Biological Sciences, The University of
Texas at El Paso, El Paso, Texas 79968-0500, USA “Centro Zamorano de Biodiversidad, Escuela Agricola Panamericana Zamorano, Departamento
de Francisco Morazadn, HONDURAS °1350 Pelican Court, Homestead, Florida 33035, USA
Abstract.—The herpetofauna of Coahuila, Mexico, is comprised of 143 species, including 20 anurans, four
caudates, 106 squamates, and 13 turtles. The number of species documented among the 10 physiographic
regions recognized ranges from 38 in the Laguna de Mayran to 91 in the Sierras y Llanuras Coahuilenses. The
individual species occupy from one to 10 regions (xX = 3.5). The numbers of species that occupy individual
regions range from 23 in the Sierras y Llanuras Coahuilenses to only one in each of three different regions. A
Coefficient of Biogeographic Resemblance (CBR) matrix indicates numbers of shared species among the 10
physiographic regions ranging from 20 between Llanuras de Coahuila y Nuevo Leon and Gran Sierra Plegada
to 45 between Serranias del Burro and Sierras y Llanuras Coahuilenses. A similarity dendrogram based on the
Unweighted Pair Group Method with Arithmetic Averages (UPGMA) reveals that the Llanuras de Coahuila y
Nuevo Leon region is most dissimilar when compared to the other nine regions in Coahuila (48.0 % similarity);
all nine other regions cluster together at 57.0% and the highest similarity is 92.0% between Laguna de Mayran
and Sierra de la Paila. The distribution patterns concerning numbers of shared species reflect higher similarity
between regions that share geographic contact with each other and have comparable ecological parameters.
The percentage of species restricted to one or two physiographic regions is 63.6%, indicating a moderately
narrow distribution for many species. The largest number of species is placed in the non-endemic category
(100), followed by the country endemics (31), state endemics (nine), and non-natives (three). The principal
environmental threats to the herpetofauna are urban development, industrial pollution, deforestation, road
effects, mining and energy projects, natural gas fracking, wind turbines, elimination due to cultural beliefs
and practices, commercial trade, and forest fires. The conservation status of the native species is assessed
by using the SEMARNAT (NOM-59), IUCN, and EVS systems, of which the EVS system proved to be the most
useful. The EVS rankings also were used to determine how species in the IUCN categories of Not Evaluated (NE)
and Least Concern (LC) might be evaluated more informatively. Using the Relative Herpetofaunal Priority (RHP)
methodology, we determined that the most significant herpetofaunas are those of the Gran Sierra Plegada and
the Sierras y Llanuras Coahuilenses. Nineteen protected areas are established in Coahuila and we predict
that 119 of the 143 species in the state occur in them, based on their respective physiographic distributions.
Finally, a set of conclusions and recommendations for the future protection of the Coahuilan herpetofauna is
presented.
Key words. Amphibians, anurans, caudates, physiographic regions, protected areas, protection recommendation,
reptiles, squamates, turtles
Resumen.—La herpetofauna de Coahuila, México consiste de 143 especies, incluyendo 20 anuros, cuatro
caudados, 106 escamosos, y 13 tortugas. El numero de especies documentadas entre las 10 regiones
fisiograficas reconocidas va de 38 en la Laguna de Mayran, a 91 en Sierras y Llanuras Coahuilenses. Las especies
individuales ocupan de una a 10 regiones (Xx = 3.5). El mayor numero de especies en una sola region va de 23 en
la Sierras y Llanuras Coahuilenses a una en cada una de las tres regiones. Una matriz de coeficiente de similitud
biogeografica (CSB) indica que el numero de especies compartidas entre las 10 regiones fisiograficas va de
20 entre Llanuras de Coahuila y Nuevo Leon y la Gran Sierra Plegada a 45 entre Serranias del Burro y Sierras
y Llanuras Coahuilenses. Un dendrograma de similitud basado en el Método por Agrupamiento de Pares no
Ponderado con Media Aritmetica (MAPMA) revela que sobre una base jerarquica, Llanuras de Coahuila y Nuevo
Leon es la mas desigual cuando se le compara con las otras nueve regiones en Coahuila (48.0% similitud);
todas las nueve regiones se agrupan en 57.0% y la mayor similitud es 92,0% entre Laguna de Mayran y Sierra
de la Paila. Los patrones de distribucion con respecto al numero de especies compartidas reflejan una mayor
similitud entre las regiones en contacto geografico y con parametros ecologicos comparables. El porcentaje
Correspondence. imantodes52@hotmail.com (DL), digitostigma@gmail.com (MNR), eligarcia_18@hotmail.com (EGP), jjohnson@utep.edu
(JDJ), vmata@utep.edu (VMS), didesantis@miners.utep.edu (DLD), bufodoc@aol.com (*LDW)
Amphib. Reptile Conserv. 31 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
de especies restringidas a una o dos regiones fisiograficas es de 63.6%, indicando una distribucion moderada
para muchas especies. El mayor numero de especies esta ubicado en la categoria de no endemica (100),
seguido de endémicas al pais (31), endémicas al estado (nueve), y no nativas (tres). Las principales amenazas
ambientales a la herpetofauna son el desarrollo urbano, contaminacion industrial, deforestacion, efectos de
carreteras, actividad minera, actividad petrolera (fracking), turbinas edlicas, matanza por falta de educacion y
para uso medicinal, colecta y comercio, e incendios forestales. Calculamos el estatus de conservacion de las
especies nativas usando los sistemas de SEMARNAT (NOM-059), UICN, y el EVS, de los cuales el EVS resulto
ser mas util. También usamos los rangos de EVS para determinar como las especies en las categorias de No
Evaluada (NE) y de Preocupacion Menor (PM) de la UICN podrian ser evaluadas de una forma mas informativa.
Asimismo, usando el método de Prioridad Herpetofaunistica Relativa (PHR), determinamos que la herpetofauna
mas significativa es la de Gran Sierra Plegada y la de Sierras y Llanuras Coahuilenses. Diecinueve areas
protegidas han sido establecidas en Coahuila y predecimos que 119 de las 143 especies que ocurren en el
estado seran encontradas en estas areas, basado en su distribuciOn geografica. Finalmente, incluimos un
grupo de conclusiones y recomendaciones para la futura proteccion de la herpetofauna de Coahuila.
Palabras claves. Anfibios, anuros, caudados, regiones fisiograficas, areas protegidas, recomendaciones de proteccion,
reptiles, escamosos, tortugas
Citation: Lazcano D, Nevarez-de los Reyes M, Garcia-Padilla E, Johnson JD, Mata-Silva V, DeSantis DL, Wilson LD. 2019. The herpetofauna of
Coahuila, Mexico: composition, distribution, and conservation status. Amphibian & Reptile Conservation 13(2) [General Section]: 31-94 (e189).
Copyright: © 2019 Lazcano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 26 January 2019; Accepted: 20 July 2019; Published: 9 October 2019
“Like it or not, and prepared or not, we are the mind Coahuila y Nuevo Leon region and the southeastern
and stewards of the living world. Our own ultimate future corner in which is found a small portion of the
depends upon that understanding.” Gran Sierra Plegada region (Fig. 1). In Mexico, the
Chihuahuan Desert also encompasses “a large portion
E. O. WILSon (2016) of the state of Chihuahua..., northeastern Durango, the
extreme northern part of Zacatecas, and small western
Introduction portions of Nuevo Leon” (https://www.worldwildlife.
org/ecoregions/nal303; accessed 24 December 2017).
Coahuila is the third largest state of Mexico after The purpose of this paper, similar to that of the others
Chihuahua and Sonora, all of which border the United — in the Mexican Conservation Series (see below), is to
States of America. Coahuila is bounded to the north by document the composition, physiographic distribution,
the US state of Texas, to the west by the Mexican states —_ and conservation status of the herpetofauna of Coahuila.
of Chihuahua and Durango, to the south by Zacatecas _In general, the format of the earlier papers in this series
and a small portion of San Louis Potosi, and to the east —_1s followed here.
by Nuevo Leon. Coahuila encompasses 151,595 km?
and falls in size between the US states of Illinois and Materials and Methods
Georgia (http://cuentame.inegi.gob.mx/monografias/
informacion/coah/default.aspx?tema=me&e=05; Our Taxonomic Position
accessed 26 August 2017). Coahuila’s population was
2,954,915 in 2015, which is 2.5% of the same-year In this paper, we follow the same taxonomic position
estimate for the entire country of Mexico (119,530,753). as explained in previous works on other portions of
Coahuila is one of the six least densely populated states | Mesoamerica (Johnson et al. 2015a,b; Mata-Silva et al.
in Mexico (the others are Chihuahua, Sonora, Campeche, 2015). Johnson (2015b) can be consulted for a statement
Durango, and Baja California Sur), each of which has __ of this position, with special reference to the subspecies
fewer than 20 inhabitants per square kilometer; the — concept.
figure for Coahuila is 19.5 (http://cuentame.ineg1.
gob.mx/monografias/informacion/coah/default. | Updating the Herpetofaunal List
aspx?tema=meé&e=05; accessed 26 August 2017). The
capital and largest city in Coahuila is Saltillo, located in = Several recent works on the herpetofauna of Coahuila
the southeastern portion of the state. are available. Lemos-Espinal and Smith (2007) created
Much of Coahuila lies within the borders of the a bilingual (Spanish and English) treatment of the state
Chihuahuan Desert (Lazcano et al. 2017), except for § herpetofauna, in which they recognized 129 species.
the northeastern portion located within the Llanuras de —__ Eight years later, Lemos-Espinal et al. (2015) compiled
Amphib. Reptile Conserv. 32 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
28°30'N
27°0'N
25°30'N
') BDM:
m™ GSP:
mI LCN:
mm LGM:
mi LSV:
mm SLC:
mi SLP:
STR:
m= SDB:
mu PSP:
TOPOGRAPHIC ASPECTS
Roads
Municipality boundaries
L_] State boundaries
4102700
ro
PHYSIOGRAPHIC REGIONS
BOLSON DE MAPIMIi
GRAN SIERRA PLEGADA
LLANURAS DE COAHUILA Y NUEVO LEON
LAGUNA DE MAYRAN
LLANURAS Y SIERRAS VOLCANICAS
SIERRAS Y LLANURAS COAHUILENSES
SIERRA DE LA PAILA
SIERRAS TRANSVERSALES
SERRANIAS DEL BURRO
PLIEGUES SALTILLO - PARRAS
Fig. 1. Physiographic regions of Coahuila, Mexico. Abbreviations are as follows: BDM = Bolson de Mapimi; GSP = Gran Sierra
Plegada; LCN = Llanuras de Coahuila y Nuevo Leon; LGM = Laguna de Mayran; LSV = Llanuras y Sierras Volcanicas; PSP =
Pliegues Saltillo-Parras; SLC = Sierras y Llanuras Coahuilenses; SLP = Sierra de la Paila; STR = Sierras Transversales.
a two-volume bilingual compendium of the herpetofauna
of three Mexican states (Chihuahua, Coahuila, and
Sonora), in which they recorded 131 species for
Coahuila. In the same year, Lemos-Espinal (2015)
edited a book on the herpetofauna found in the states
along the Mexico-US border, and recorded 133 species
for Coahuila. Finally, Lemos-Espinal and Smith (2016)
produced a checklist of the Coahuila herpetofauna, in
which they again reported 133 species for the state. The
name usages indicated in the Taxonomic List located at
Amphib. Reptile Conserv.
33
the Mesoamerican Herpetology website (http://www.
mesoamericanherpetology.com; accessed 8 March 2018)
are followed here.
System for Determining Distributional Status
The system developed by Alvarado-Diaz et al. (2013) for
the herpetofauna of Michoacan is employed to ascertain
the distributional status of members of the herpetofauna
of Coahuila. Mata-Silva et al. (2015), Johnson et al.
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
er
Fig. 2. Bolsén de Mapimi. Vegetation in the Bolsoén de Mapimi, in the municipality of the same name in the neighboring state of
Durango. Photo by Gabriel Viesca Ramos.
(2015a), Teran-Juarez et al. (2016), Woolrich-Pifia et al.
(2016, 2017), Nevarez-de los Reyes et al. (2016), Cruz-
Saenz et al. (2017), and Gonzalez-Sanchez et al. (2017)
used this system, which consists of the following four
categories: SE = endemic to Coahuila; CE = endemic to
Mexico; NE = not endemic to Mexico; NN = non-native
in Mexico.
Systems for Determining Conservation Status
Assessment of the conservation status of the herpetofauna
of Coahuila, employed the same systems (.e.,
SEMARNAT, IUCN, and EVS) used by Alvarado-Diaz
et al. (2013), Mata-Silva et al. (2015, 2019), Johnson et
al. (2015a,b), Teran-Juarez et al. (2016), Woolrich-Pifia
et al. (2016, 2017), Nevarez-de los Reyes et al. (2016),
Cruz-Saenz et al. (2017), Gonzalez-Sanchez et al. (2017),
and DeSantis et al. (2018). Detailed descriptions of these
three systems appear in earlier papers in this series.
The Mexican Conservation Series
The Mexican Conservation Series (MCS) was initiated
in 2013, with a study of the herpetofauna of Michoacan
(Alvarado-Diaz et al. 2013), as a part of a set of five papers
designated as the Special Mexico Issue published in
Amphibian & Reptile Conservation. The basic format of
the entries in the MCS was established in that paper, 1.e.,
to examine the composition, physiographic distribution,
and conservation status of the herpetofauna of a given
Mexican state or group of states. Two years later, the
MCS was continued with papers on the herpetofauna of
Oaxaca (Mata-Silva et al. 2015) and Chiapas (Johnson
Amphib. Reptile Conserv.
et al. 2015a). In the ensuing year, three entries in the
MCS appeared, those on Tamaulipas (Teran-Juarez et al.
2016), Nayarit (Woolrich-Pifia et al. 2016), and Nuevo
Leon (Nevarez-de los Reyes et al. 2016). Finally, three
entries on Jalisco (Cruz-Saenz et al. 2017), the Mexican
Yucatan Peninsula (Gonzalez-Sanchez et al. 2017), and
Puebla (Woolrich-Pifia et al. 2017) appeared. Thus, this
paper on the herpetofauna of Coahuila is the 10" entry in
this series.
Physiography and Climate
Physiographic Regions
The classification system of physiographic regions
(= subprovinces) developed by INEGI in 2004 was
used to analyze the distribution of the herpetofauna of
Coahuila. This system consists of 10 regions (Fig. 1),
which are briefly described below (see INEGI, http://
www. inegi.org.mx/est/contenidos/proyectos/ce/ce2004/
presentacion.aspx).
Bolsén de Mapimi (BDM). This region, which
encompasses 4,715 km? (3.1% of the state area), is
entirely confined within Mexican territory and runs along
the Sierra Madre Occidental, eventually expanding to the
east in the Mapimi zone. Plains and bajadas dominate
the landscape, although small sierras and lomerios facing
north-south are also found there. The sierras and lomerios
located to the north are composed predominantly of
volcanic rocks and are found associated with faults on
their flanks; to the south limestone is the most abundant
rock. The northern portion of the region is transected by
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Fig. 3. Gran Sierra Plegada. Vegetation in the vicinity of Monterreal in the municipality of Arteaga. Photo by Eli Garcia-Padilla.
the Rio Florido and its effluents, and tributaries of the
Rio Conchos; the southern portion is crossed by the Rio
Nazas. Superficial water sources, however, are scarce.
The Bolson de Mapimi is a flat region at elevations
around 1,200 m, located between Sierra del Diablo, Sierra
Mojada, and irrigation district no. 17. The latter region,
also known as the Comarca Lagunera or La Laguna, used
to be inundated every summer by the waters of the Rio
Nazas until the construction of the Reservoir Francisco
Zarco in the state of Durango. The arid plains of Mapimi
are interrupted by low geomorphological features such
as sand dunes in the northeastern portion. Deep soils of
alluvial or lacustrine origin are well-represented in the
plains. Most of the original vegetation around Torreon,
Matamoros, and San Pedro de las Colonias has been
replaced by agricultural fields. A section of the region
in Laguna del Rey, however, contains microphyll desert
scrub; and a similar habitat is found in the ridges of
Mojada and Montafia del Rey. The middle of this region
contains sand dunes, and the vegetation consists primarily
of Gobernadora/Creosote Bush (Larrea tridentata) and
huizaches (Vachellia [Acacia] spp.), providing minimum
surface cover. The landscapes at La Laguna and El Guaje
are represented by halophytic vegetation, and of less
importance are small areas of grassland and scrubland
where the main plant species is L. tridentata.
Llanuras y Sierras Volcanicas (LSV). This region covers
approximately 14,000 km?(9.2%) of the state of Coahuila,
with elevations ranging between 600 m and 1,200 m. The
largest area of this territory 1s represented by plains or
bajadas; these flat surfaces are more prominent and less
Amphib. Reptile Conserv.
35
disrupted at Llano de los Ranchos, south of the mountain
ranges that rise along the Rio Bravo/Grande and at
Bolson de los Lipanes to the north of Sierra Mojada.
This region includes small sierras of volcanic rock, such
as Sierra el Mulato, Ocotillo, and Hechicero, located to
the southeast of Ojinaga and the banks of the Rio Bravo.
Small mountains of limestone arise at the southern edge
border with Bolson de Mapimi, as in La Mojada and El
Diablo. Some streams originating in this region feed the
Rio Bravo, and some accumulate water for short periods
of time, but the climate regime 1s that of a desert.
The landscape in this region is dominated by shrubs,
which are generally shorter than two m. Microphyll desert
scrub is found with some variations in its components,
with plains and slopes mostly vegetated by Gobernadora
(L. tridentata), Viscid Acacia/Huizache (Vachellia
vernicosa), Ocotillo (Fouquieria splendens), and mesquite
(Prosopis spp.), there are also other vegetation elements,
such as gatufio/Mimosa (Mimosa spp.), Purple Prickly-
pear (Opuntia macrocentra), and a minor proportion
of huizaches reaching heights of less than 1.5 m. The
components of the lower strata are Cenizo (Leucophyllum
jrutescens), Mariola (Parthenium incanum), Hierba del
Burro/Zinnia (Zinnia acerosa), and Plumed Crinklemat
(Tiquilia greggii). Arborescent yuccas (Yucca spp.) and
Viscid Acacia (V. vernicosa) also are found, reaching
heights of more than four m. This community is widely
distributed in the region, in all the bajadas that feed the
lagoon El Guaje and the western plains.
Laguna de Mayran (LDM). Laguna de Mayran covers
7,804 km? (5.1%) of the state, and is mostly represented
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
No. 1. Anaxyrus speciosus (Girard, 1854). The Texas Toad is distributed from “southeastern New Mexico and western Oklahoma
(USA) south throughout central and West Texas to central Tamaulipas, northern Nuevo Leon, northern and eastern Coahuila, and
northeastern Chihuahua” in Mexico (Frost 2018). This individual came from Allende, in the municipality of Allende. Wilson et al.
(2013b) calculated its EVS as 12, placing it in the upper portion of the medium vulnerability category. Its conservation status has
been considered as Least Concern by IUCN, but this species is not listed by SEMARNAT. Photo by Michael S. Price.
No. 2. Craugastor augusti (Duges, 1879). The Common Barking Frog occurs from “Arizona to Texas in the United States, and
in Mexico from Sonora to Oaxaca, and from Chihuahua, Coahuila, Nuevo Leon, and Tamaulipas to Puebla” (Lemos-Espinal and
Dixon 2013: 42). This individual was found at Cuatrociénegas in the municipality of Cuatrociénegas de Carranza. Wilson et al.
(2013b) ascertained its EVS as 8, placing it in the upper portion of the low vulnerability category. Its conservation status has been
evaluated as Least Concern by IUCN; this species is not listed by SEMARNAT. Photo by Michael S. Price.
Amphib. Reptile Conserv. 36 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
No. 3. Lithobates berlandieri (Baird, 1859). The Rio Grande Leopard Frog ranges from “central and western Texas and southern
New Mexico (USA) through eastern Chihuahua to central Veracruz and Hidalgo, Mexico; introduced into the lower Colorado River
and lower Gila River drainages of Sonora and Baja California del Norte, Mexico, and California and Arizona, USA.” (Frost 2018).
This individual was found at El Oso, in the municipality of Cuatrociénegas de Carranza. Wilson et al. (2013b) calculated its EVS
as 7, placing it at the middle portion of the low vulnerability category. Its conservation status has been considered as Least Concern
by IUCN, and as a species of special protection (Pr) by SEMARNAT. Photo by Michael S. Price.
_ el
No. 4. Barisia ciliaris (Smith, 1942). The Sierra Alligator Lizard is a Mexican endemic distributed “along the Sierra Madre Oriental
from Nuevo Leon and southeastern Coahuila southward to at least Guanajuato, and northward along the Sierra Madre Occidental
to extreme southern Chihuahua” (Lemos-Espinal and Dixon 2013: 97). Pictured here is an individual encountered near Monterreal,
in the municipality of Arteaga. Wilson et al. (2013a) determined its EVS to be 15, placing it in the lower portion of the high
vulnerability category. Its conservation status has not been assessed by IUCN, and this species is not listed by SEMARNAT. Photo
by Eli Garcta-Padilla.
i
Amphib. Reptile Conserv. 37 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
by grassland and some hills found in the municipalities of
Francisco I. Madero, General Cepeda, Parras, San Pedro,
and Viesca. This region includes endorheic terminal
basins of the Nazas and Aguanaval rivers. These rivers
emerge in the Sierra Madre Occidental province, and
flow northward through the province of Mesa del Centro
to the Mayran lagoon. The region is mostly represented
by two bodies of water, Laguna de Mayran, formerly fed
by the Nazas and Viesca rivers, and Laguna de Viesca,
a smaller water body fed by the Aguanaval River. Both
lagoons are located at an elevation of ca. 1,400 m, with
a west-east orientation, and are separated from each
other by a phalanx of the Sierra Madre Oriental. Until
recently, these deposits used to store a significant amount
of water for most of the year, but currently their nearly
level surfaces have turned into desert plains, with saline
areas at the center of the Mayran lagoon and almost
the entire Viesca lagoon. Their disappearance as lakes
and their final passage to a desert regime are the result
of reservoirs and canal systems built on the Nazas and
Aguanaval rivers for irrigation of the Laguna district;
activities that, on the other hand, have significantly
increased productivity in other areas.
Halophytic vegetation is the dominant element of
the landscape, as the soils contain high concentrations
of salts. In fact, roughly from San Pedro de las Colonias
to the boundaries of the Mayran lagoon and throughout
the region, there is no other component than halophytic
vegetation. The area around Mesa Albardienta is
completely devoid of vegetation due to hypersaline
conditions in the soil. Halophytic vegetation in this region
is represented by Saladillo/Salt Bushes (Azriplex spp.),
Seepweeds (Suaeda spp.), and Dropseed (Sporobolus
spp). Besides these types of vegetation, there are small
areas with microphyll desert scrub and rosette scrub in
the Sierrita San Lorenzo.
Sierras y Llanuras Coahuilenses (SLC). This region
covers 43,937 km? (29.0%) of the state. It includes
the municipalities of Abasolo, Frontera, Lamadrid,
Nadadores, Sacramento, and San Buenaventura, as well
as parts of Acufia, Candela, Castafios, Cuatrociénegas,
Escobedo, Monclova, Muzquiz, Ocampo, Progreso, and
Ramos Arizpe, and very small portions of San Juan de
Sabinas and Zaragoza. It consists of folded limestone
mountains ranges, oriented northwest to southeast,
mostly with steep small folds. Most of the mountains lie
between elevations of 1,000 to 2,000 m, although peaks
with elevations over 2,000 m can be found only in Sierra
El Carmen and Sierra de San Antonio. The region has
mostly internal drainage, so its runoff contributions to
the Rio Bravo are minimal.
Vegetation types present in the region are submontane
scrub, chaparral, microphyll desert scrub, and rosette
scrub. The chaparral is generally a dense shrub
community, which is distributed in the transition zone
between the arid scrubland and forests. In this region, it
Amphib. Reptile Conserv.
represents an intermediate layer between the submontane
shrubs and forest, and is also frequently found mixed as
chaparral and desert scrub. It is composed of shrubby
oaks (Quercus spp.) and shrub species in the genera
Cercocarpus and Vauquelinia, among others. Other
shrub components such as sotols (Dasylirion spp.) and
yuccas (Yucca spp.) are also present.
Serranias del Burro (SDB). This region encompasses
13,234 km? (8.7%) of the state, and includes parts of the
municipalities of Acufia, Guerrero, Muzquiz, Sabinas,
Villa Union, and Zaragoza, as well as very small portions
of Juarez, Morelos, and San Juan de Sabinas. The
Serranias del Burro has a normal fault on its northwestern
flank. It is rugged in its central part, which includes a
radial system of narrow valleys, but lies much more
towards the east and southeast, where the sierra becomes
narrow and descends into the hilly zone of Peyotes. A
series of igneous intrusions crosses the Serranias del
Burro from east to west near Villa Acufia and Cerro El
Colorado, with the latter representing the highest peak
of the mountain range, with an elevation of 1,400 m.
The region has few major streams, although it has slopes
toward the Rio Bravo. Soils in the topoform systems
(sierras) constituting this region are mainly represented
by shallow lithosols, while xerosols, phaeozems, and
regosols cover the small systems of hills (lomerios).
Soils on slopes (bajadas) have colluvial or colluvial-
alluvial sources, and the edaphic landscapes in the
intermontane valleys of the Serranias del Burro are very
similar to those in the other regions mentioned above.
The vegetation types found in this region are typical of
the arid zones of Mexico. The hilly zones (lomerios)
that border the mountains of Colorado, del Burro, and
La Babia are covered with rosette scrub. Among the
main components of this vegetation are Lechuguilla
(Agave lechuguilla), Texas Sotol (Dasylirion texanum),
and short yuccas (Yucca spp.). Submontane shrubs on
the Serranias del Burro also ascend the eastern slopes of
the range, with the most distinctive components being
Cenizo/Purple Sage (Leucophyllum frutescens), Tenazas
(Havardia pallens), Hoja Ancha/Tarbush (Flourensia
laurifolia), and Coyotillo/Buckthorn (Karwinskia sp.).
Another vegetation formation of great importance in the
region is chaparral, which grows below the oak forest
on the Sierras del Burro, del Carmen, and La Babia;
this vegetation also grows on the small hills located
immediately to the north of these mountain ranges.
There is also a large number of pine forests in this
region, numerically dominated by Pino Pifionero (Pinus
cembroides). Additionally, there are large extensions of
grassland in the intermontane valleys immediately below
the chaparral.
Finally, in the lower portion of the sierras, adjacent to
the Great Plains of North America, there is Tamaulipecan
thorn scrub. This vegetation is located on the hills
to the south of the region bordering the rosette scrub
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
found on the hills of Peyotes. The main components
of this vegetation formation are Palo Verde (Cercidium
texanum), Chaparro } Amargoso/Indian Paintbrush
(Castela texana), Cenizo (Leucophyllum frutescens), and
mesquite trees (Prosopis spp. ).
Sierra de la Paila (SLP). This region includes sierras,
large bolsons with internal drainage, and bajadas. It covers
ca. 19,230 km? (12.7%) of the state. Valle Buenavista
bolson is located in the western portion, bordered to
the west by Sierra de Tlahualilo and to the east by the
highlands of Albardienta, which reach an elevation of
1,800 m. Sierra de La Paila is located to the east, and the
bolsons El Sobaco, El Hundido, San Marcos, and Los
Pinos are located to the north, with the first three at less
than 1,000 m elevation. As in the other regions, the soils
and biodiversity in the Sierra de La Paila is influenced by
climate, which is semiarid at high elevations and very arid
in the grasslands and bolsons. Although topographically
rugged, the sierras have relatively small portions covered
with soils. There are, however, deep soils of primarily
alluvial origin in the lower sections of the bolsons that
have high concentrations of salts. Also, there are sandy
soils of eolic origin that form dunes.
The vegetation communities in this region are mostly
the same as those in Sierras Transversales and Pliegues
Saltillo-Parras. Microphyllous and rosette scrub is
closely associated with the terrain, and dry and semidry
climatic conditions are present in the bajadas and valleys.
Rosette scrub is widely distributed in all sierras such as
La Fragua, La Mesa Albardienta, and La Paila. Chaparral
is a community of shrubs primarily represented by oaks
(Quercus spp.), Chapote/Texas Persimmon (Diospyros
texana), and some elements of rosette scrub, like
yuccas, Sotol, and Lechuguilla. Submontane shrub is
a community composed of shrubs, primarily Chapote
(D. texana), Tenazas (H. pallens), Guajillo (Acacia
berlandieri), and Chaparro Prieto (Acacia amentacea).
These shrubs are also found in La Paila and La Fragua at
the same elevations as chaparral.
Pliegues Saltillo—Parras (PSP). This region covers 9,195
km? (6.1%) of the state of Coahuila. The landscape is
represented by a set of valleys extending from east to
west, situated at an elevation of approximately 1,600 m
and bordered to the north and south by eroded flanks and
valleys. The region also includes the Sierra de Parras,
on which peaks can reach more than 3,000 m, and
includes a succession of truncated large flanks toward
the south. This region in Coahuila includes parts of
the municipalities of Parras, Cepeda, Saltillo, Arteaga,
Ramos Arizpe, Castafios, Candela, and Monclova.
Microphyll desert scrub and rosette scrub are
the dominant vegetation types in this area. Rosette
scrub is distributed on mountain ranges, slopes, and
hills, especially in shallow soils, and alternating with
microphyll scrub in flatter areas, in deep and alluvial soils.
Amphib. Reptile Conserv.
To the north of San Martin de las Varas, rosette scrub
contains some representatives of Pinus cembroides, but
they do not modify the physiognomy of this vegetation
community. Pine forests are also found in the southern
part of the region, on the bajadas of the Sierra El Jabali,
where their density increases with elevation. Between
the scrub and forest, there are two types of natural and
introduced grassland areas. The first area is located south
of General Cepeda, and to the south of Saltillo on the
hills next to Estacion Agua Nueva, and contains grasses
of the genera Bouteloua and Sporobolus. Introduced
grasslands are found to the east of Saltillo, through a
substantial geographic extension of grasses belonging to
the genera Bouteloua and Aristida.
Sierras Transversales (STR). This region extends
throughout the southern section of the state, in the
municipalities of Cuatro Ciénegas, Ocampo, and Sierra
Mojada, encompassing a surface area of 14,077 km? (9.3%
of the state area). Over half of this region consists of sierras
with shallow light-colored soils. The main vegetation
is represented by rosette scrub and microphyll desert
scrubland. Rosette scrub vegetation is distributed on all
the mountains, slopes, and small hills located at elevations
between 2,000 and 2,400 m, with large portions of this
vegetation located on the sierras El Numero, Candelaria,
Parras, and other smaller sierras. The main components of
this vegetation are Huizache (Acacia farnesiana), Chapotes
(D. texana), Texas Sotol (D. texanum), Lechuguilla (A.
lechuguilla), and Gatufio (Acacia roemeriana). In the
lower parts of the sierras Playa Madero and del Laurel,
the same type of vegetation is also found, where the
numerically dominant Yucca thompsoniana gives the
appearance of an Izotal (Yucca tree forest), in addition to
Sotol, Lechuguilla, Chaparro Prieto (Acacia rigidula), and
Fresno (Fraxinus greggii), among others. This association
also is present on the bajadas of the sierras.
The abundance of microphyll shrubs is noteworthy
on flat areas, especially in the southeastern part of the
state, with thorny elements present, such as mesquites
(Prosopis spp.) and huizaches (Acacia spp.), as well as
Gobermadora (L. tridentata) and Hojasén (Fluorencia
cernua). Additionally, relatively small areas of grassland
are found on the sierras of GOmez Farias and Jabali,
with species of the genera Bouteloua, Muhlenbergia,
Andropogon, and Aristida. The southeastern section of
the state also has flat areas with halophytic vegetation
on saline soils, with species of saladillo (Suwaeda spp.)
and saltbushes (Atriplex spp.). On the other hand,
chaparral, pine-oak forest, pine forest, and small areas
with submontane scrub are found in the less arid sierras,
such as the Sierras de Jimulco, Parras, and Jabali. Among
components of the chaparral are small oaks (Quercus
spp.) and Pino Pifionero (P. cembroides).
Gran Sierra Plegada (GSP). This region covers 2,178
km? (1.4%) of the state. It includes a major portion of the
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 1. Monthly minimum, mean (in parentheses), maximum, and annual temperature data (in °C) for the physiographic regions of Coahuila, Mexico. The locality and
elevation for each region are: Bolson de Mapimi
Laboratorio del Desierto, Tlahualilo, Durango (1,160 m); Llanuras y Sierras Volcanicas
Laguna de Mayran—Viesca (1,100 m); Sierras y Llanuras Coahuilenses—San Francisco Nadadores (500 m); Serrania del Burro—Agua Nueva (370 m); Sierra La Paila
Sierra Mojada (1,256 m);
Hipolito (1,150 m); Pliegues Saltillo-Parras—General Cepeda (1,400 m); Sierras Transversales—La Ventura (1,867 m); Gran Sierra Plegada—San Antonio de las Alazanas
(2,300 m); and Llanuras de Coahuila y Nuevo Le6n—Presa Venustiano Carranza (272 m). Data from: http://www. smn1.conagua.gob.mx/climatologia/normales/estacion/
EstacionesClimatologicas.kmz; accessed 11 November 2017.
Physiographic Region Jan Feb Mar Apr May
Bolson de Mapimi 3.0 5.0 8.2 12.4 16.5
(11.7) (14.0) (17.4) (21.5) (25.3)
20.3 23.0 26.7 30.6 34.1
Llanuras y Sierras 4.3 De 8.2 12.0 15.0
Volcanicas (10.6) (12.2) (15.6) (19.5) = (22.6)
16.8 18.9 23.0 27.0 30.3
Laguna de Mayran 40 6.2 9.0 13.0 16.7
(14.0) (16.4) (19.6) (23.3) (26.7)
24.0 26.7 30.3 33.6 36.6
Sierras y Llanuras 2.8 47 7.5 1 Ui 16.3
Coahuilenses (11.0) (14.0) (17.4) (21.5) ~~ (25.7)
19.3 233 212 31.6 35.2
Serrania del Burro 46 5.0 7.5 123: 15.7
(11.7) (12.7) (15.8) (20.7) (23.8)
18.9 20.5 24.0 29,2, 31.9
Sierra La Paila 9.6 10.7 12.8 14.5 17.6
(15.0) (16.0) (17.9) (20.2) (23.0)
20.3 21:3 23.1 25:9 28.3
Pliegues Saltillo-Parras 5.3 6.5 9.4 12.9 15.8
(12.8) (14.4) (17.9) (21.2) (24.0)
20.2 223 263 29.5 32.1
Sierras Transversales 19 em a3 Le 10.9
(11.7) (13.1) = (16.0) (18.5) (21.6)
21.5 23-1 26.8 29.4 32.3
Gran Sierra Plegada 42 5.0 6.2 7.8 9.0
(12.2) (13.2) (14.6) (16.4) (17.5)
20.2 21.3 22.9 25. 25.9
Llanuras de Coahuila y 49 7.0 10.7 15.1 19.0
Nuevo Leon (11.9) (14.5) (18.5) (22.8) ~—_ (26.0)
18.9 22-0 26.2 30.5 33.1
municipality of Arteaga (95%) and a very small fraction of
Saltillo. This region begins east of Saltillo, Coahuila, but also
includes sections in Nuevo Leon, Tamaulipas, and San Luis
Potosi, and is dominated by folded layers of limestone. A
great reverse geological fault lies on the eastern edges of the
Gran Sierra Plegada, while smaller ones extend relatively
parallel to it and its structural axes. The elevational range in
the region is between 2,000 and 3,750 m.
The topography is predominantly mountainous, but
also contains plateaus and valleys. This region 1s located
somewhat parallel to the Gulf of Mexico and represents an
orographic barrier that favors the deposition of moisture
on the eastern slopes, which prevents the westward
movement of moist winds. Heavy rainfall has led to the
dissolution of limestone rocks in the area, resulting in
a karstic environment. These processes have led to the
formation of vast cavern systems and springs at the foot
of the mountains. A broad elevational gradient is present
in this area. The soils are dominated by lithosols, which
are associated with rendzinas and calcaric regosols.
Amphib. Reptile Conserv.
Jun Jul Aug Set Oct Nov Dec
19.1 19.2 18.6 16.7 12.7 TS 33
(27.2) (26.5) (25.8) (23.8) (20.6) (15.8) (12.0)
35.3 33,9 33.0 31.0 28.5 24.2 20.6
16.7 16.4 16.0 14.1 11.0 7.0 49
(24.3) (23:5) (22:9) (20.8) (17.9) (14.1) (11.1)
31.8 30.5 29-7, 215 24.9 971 Uh | 17.4
19.5 20.2 195 18.0 13.4 7.7 46
(28.3) (28.1) (27.6) (26.0) (22.4) (17.8) (14.4)
37.1 36.0 35.7 33.9 31.5 27.8 24.2
19:2 19,2 20%) 17.0 12:5 Tee 41
(28.0) (27.8) (28.3) (24.8) (20.7) (15.8) (12.1)
36.7 36.3 36.5 Sap 28.8 24.3 20.2
18.4 18.8 18.9 16.3 a Tad 44
(25.8) (25.8) (25.1) (22.8) (18.6) (14.5) (10.6)
33.3 32.8 33 292 25:1 212 16.7
19.5 19.5 19.4 17.6 15.9 13.1 11.1
(25.1) (25.2) (24.8) (22.6) (21.0) (18.4) (16.1)
30.8 30.9 30.2 27.6 26.1 23.6 211
17.5 17.4 16.9 15.0 12.2 8.4 6.2
(25.0) (24.6) (24.0) (21.8) (19.5) (15.9) (13.5)
32.5 31.8 31.0 28.6 26.7 23.4 20.8
(bees) 13.3 12.6 12.2 8.8 5.6 2.1
(22.5) (22.3) (21.7) (21.5) (19.4) (15.5) (12.0)
32.6 31.3 30.8 30.8 29.9 255 21.9
9:5 9.6 9.1 8.6 2 5.6 46
(17.5) (17.3) (16.9) (16.6) (15.6) (14.2) (12.7)
25.5 24.9 24.4 24.6 23.7 22:9 20.7
21.7 22.6 po) 20.3 15:7 9.8 5.6
(28.7) (29.5) (29.3) (26.7) (22.3) (16.8) (12.8)
35:7, 36.5 36.1 33.1 28.9 23.8 19.9
Calcic and haplic xerosols are also found within the
region.
In general, two fundamental forms of plant landscapes
are present in the region: forests and scrublands. Pines
dominate the forested area, and desert rosette scrub,
piedmont scrub, and chaparral dominate the rest of the
region. Other types of vegetation in the Gran Sierra
Plegada occur as small patches of grassland, halophytic
vegetation, or alpine prairie, but they have minimal
influence in shaping the overall landscape.
Llanuras de Coahuila y Nuevo Leon (LCN). This region
encompasses 25,666 km? (16.9% of the state area),
including the municipalities of Hidalgo, Nava, Piedras
Negras, and Jiménez, and parts of Guerrero, Villa Union,
Morelos, Allende, Progreso, Escobedo, Sabinas, San
Juan de Sabinas, Nueva Rosita, Muzquiz, Zaragoza,
and Acufia. The region is characterized by the presence
of plains interrupted with scattered low hills that are
composed of conglomerates, at elevations ranging from
40 October 2019 | Volume 13 | Number 2 | e189
Annual
11.8
(20.1)
28.4
10.9
(17.9)
24.9
12.7
(22.1)
31.5
11.9
(20.6)
29.3
11.8
(19.0)
26.2
15.1
(20.4)
25.8
12.0
(19.6)
27.1
8.0
(18.0)
28.0
72
(15.4)
23.5
14.6
(21.7)
28.7
Lazcano et al.
Fig. 4. Llanuras de Coahuila y Nuevo Leon. Tamaulipas thorn
scrub in the municipality of Allende. Photo by Manuel Nevarez
de los Reyes.
Fig. 6. Llanuras y Sierras Volcdnicas. Vegetation near Heér-
cules, in the municipality of Sierra Mojada. Photo by Daniel
Solorio Estrada.
75 to about 500 m. One of the most extensive plains
extends from Anahuac, Nuevo Leon, to Nueva Rosita,
Coahuila, at an average elevation of 500 m.
Tamaulipan thornscrub and mesquites (Prosopis spp.)
are the most characteristic vegetation types in this region.
Tamaulipan thornscrub is distributed at elevations from 80
to 340 m, witha physiognomy of thornscrub in areas of low
relief and of semi-thorn scrubland on the lower sections
of areas with higher relief. Large patches of Cenizo (L.
frutescens) are present in some areas, indicative of a high
degree of disturbance to the native scrub vegetation, as
this species numerically dominates the sympatric native
species that are found in low frequency and are small in
size. Mesquites dominate at elevations from 75 to 400 m.
Piedmont scrub or Tamaulipan thornscrub predominate
in some middle sections, and a prevalence of halophytic
elements is present in the lower areas. Some deciduous
thornscrub and deciduous hardwood forests are found in
the region as well, and oak and pine-oak forests occur at
higher elevations. Halophytic vegetation is found within
small areas of the plains and valleys, where high salt
concentrations are present in the soils. Natural grassland
Amphib. Reptile Conserv.
41
Fig. 5. Laguna de Mayrdn. Vegetation on Cerro de la Virgen,
in the municipality of Parras. Photo by José Flores Ventura.
SE UAW Dee eg tte ee ae
Fig. 7. Pliegues Saltillo-Parras. Vegetation near Parras de la
Fuente, in the municipality of Parras. Photo by Manuel Nevdrez
de los Reyes.
occurs in some areas of the plains at elevations from 135
to 290 m. The introduced grasses on the plains and valleys
are composed primarily of Buffelgrass (Pennisetum
ciliare), which 1s distributed at elevations from 190 to
270 m and covers small hilly areas and alluvial plains.
Climate
Temperature. The minimum, mean, and maximum
temperatures for one locality in each of the 10
physiographic regions in Coahuila are shown in Table 1.
The elevations for these 10 regions range from 272 m in
the Llanuras de Coahuila y Nuevo Leon to 2,300 m in the
Gran Sierra Plegada.
The mean annual temperature (MAT) of these regions
ranges from a low of 15.4 °C, in the Gran Sierra Plegada
at 2,300 m in the southeastern portion of the state, to a high
of 22.1 °C, in the Laguna de Mayran at 1,100 m in the
southern portion of the state. The MAT of these regions in
Coahulia are unusual tn that they do not gradually decrease
with increasing elevation. The MAT lie below 20 °C in
four additional regions, including the Llanuras y Sierras
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 2. Monthly and annual precipitation data (in mm) for the physiographic regions of Coahuila, Mexico. The locality and elevation
for each region are: Bolson de Mapimi—Laboratorio del Desierto, Tlahualilo, Durango (1,160 m); Llanuras y Sierras Volcanicas—
Sierra Mojada (1,256 m); Laguna de Mayran—Viesca (1,100 m); Sierras y Llanuras Coahuilenses—San Francisco Nadadores (500
m); Serrania del Burro—A gua Nueva (370 m); Sierra La Paila—Hipolito (1,150 m); Pliegues Saltillo-Parras—General Cepeda (1,400
m); Sierras Transversales—La Ventura (1,867 m); Gran Sierra Plegada—San Antonio de las Alazanas (2,300 m); Sierras y Llanuras
Occidentales—Carbonera, Galeana, Nuevo Leon (2,035 m); and Llanuras de Coahuila y Nuevo Leon—Presa Venustiano Carranza
(272 m). The shaded area indicates the months of the rainy season. Data from: http://www. smn1.conagua.gob.mx/climatologia/
normales/estacion/EstacionesClimatologicas.kmz; accessed 11 November 2017.
PBoiséndeMapimi | 95 [40 | 42 | 89 | 152 | 362 | 466 | 548] a4 [208] 91 | 69 | 2586 |
[sierataPaila ——-| 90 [91 | 8 | 82 | 168 | aso [291 | 23 | an7 | 27 | se | 86 | i681 |
Volcanicas at 1,256 m (17.9 °C), the Serranias del Burro
at 370 m (19.0 °C), the Pliegues Saltillo-Parras at 1,400 m
(19.6 °C), and the Sierra Transversales at 1,867 m (18.0°C).
In contrast, the MAT in the remaining five regions lie
above 20 °C, including the Bolson de Mapimi at 1,160 m
(20.1 °C), the Laguna de Mayran at 1,100 m (22.1°C), the
Sierra de Paila at 1,150 m (20.4 °C), the Sierras y Llanuras
Coahuilenses at 500 m (20.6 °C), and the Llanuras de
Coahuila y Nuevo Leon at 272 m (21.7 °C).
The minimum annual temperature ranges from 7.2
°C in the Gran Sierra Plegada to 15.1 °C in the Sierra
La Paila (Table 1). The maximum annual temperature
varies from 23.5 °C in the Gran Sierra Plegada to 31.5
°C in the Laguna de Mayran. The minimum annual
temperature is 10.7—20.0 °C lower than the maximum
annual temperature among the 10 physiographic regions
of the state (Table 1). Mean monthly temperatures peak
at some point from May to August, usually June, and
reach a low point sometime during December or January,
usually January (Table 1).
Precipitation. As expected, precipitation in Coahuila is
generally highest during the rainy season from June to
October, and lowest from November to May, during the
dry season. The data in Table 2 indicate that 56.8—-77.6%
(x = 69.4%) of the rainfall occurs during the rainy season.
Table 3. Composition of the native and non-native herpetofauna
of Coahuila, Mexico.
The month with the greatest amount of precipitation,
depending on the location, is June, July, August, or
September, usually August (Table 2). The month with
the least amount of precipitation, again depending on
the location, is December, February, or March, usually
March (Table 2). The annual precipitation ranges from
96.9 mm in the Serranias del Burro to 384.3 mm in the
Llanuras de Coahuila y Nuevo Leon.
Composition of the Herpetofauna
Families
The herpetofaunal species of Coahuila are placed
in 28 families, including seven for anurans, two for
salamanders, 15 for squamates (one of which contains
only a single non-native species), and four for turtles
(Table 3). The seven anuran families comprise 63.6% of
the 11 families with representatives in Mexico. The two
salamander families constitute 50.0% of the four families
represented in the country. The fifteen squamate families
make up 48.4% of the 31 Mexican families containing
native species. Finally, the four Coahuilan turtle families
encompass 40.0% of the 10 families in Mexico. The total
of 28 families includes 47.5% of the 59 herpetofaunal
families that are represented in this country (Johnson et
al. 2017). There are no caecilian or crocodylian families
with representatives in Coahuila.
Orders Families Genera Species Genera
Anura 7 13 20
Caudata 2 3 4 Sixty-six herpetofaunal genera are represented
Subtotals 9 16 74 in Coahuila, including 13 for anurans, three for
Squamata 15 44 106 salamanders, 44 for squamates, and six for turtles (Table
Testudines 4 6 13 3). The 13 anuran genera constitute 35.1% of the 37
Subtotals 19 50 119 with representatives in Mexico. The three salamander
Totals 28 66 143 genera make up 15.8% of the 19 found in Mexico. Of the
Amphib. Reptile Conserv.
42
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
rm ¥ 7. valu. # “et fy ae ;
No. 5. Gerrhonotus infernalis Baird, 1859. The Texas Alligator Lizard ranges “from central Texas westward to the area of Big Bend,
in the United States, and in Mexico east of the Sierra Madre Oriental to southern San Luis Potosi and perhaps extreme southeastern
Durango” (Lemos- Espinal and Dixon 2013: 98). This individual was found in Sierra La Concordia, in the municipality of General
Cepeda. Wilson et al. (2013a) calculated its EVS as 13, placing it at the upper end of the medium vulnerability category. Its
conservation status has been gauged as Least Concern by IUCN, and this species is not listed by SEMARNAT. Photo by Michael
S. Price.
4
a. lal _ . S
= A
es - >
b Soap --'* . ¢ : a &
* ; ; ,
7 J : «fT - . * p- : . 7 ~
4, - * «
w eb . -— : : oe ba
No. 6. Gerrhonotus lugoi McCoy, 1970. Lugo’s Alligator Lizard is a Mexican endemic species restricted to the Cuatro Ciénegas
region (Lemos-Espinal et al. 2015). This individual was found at Cuatrociénegas, in the municipality of Cuatrociénegas de Carranza.
Wilson et al. (2013a) judged its EVS as 17, placing it in the middle portion of the high vulnerability category. Its conservation status
is evaluated as Least Concern by IUCN, and as threatened (A) by SEMARNAT. Photo by Michael S. Price.
Amphib. Reptile Conserv. 43 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
a\, & vs Pa Se
2 See Ps
No. 7. Gerrhonotus mccoyi Garcia-Vazquez, Contreras-Arquieta, Trujano-O
ega, and Nieto-Montes de Oca, 2018. McCoy’s
Alligator Lizard is a Mexican endemic species restricted to the Cuatro Ciénegas region (Garcia-V a4zquez et al. 2018). This individual,
a male paratype of the species, was encountered at Pozas Azules, Rancho Pronatura in the municipality of Cuatro Ciénegas. The EVS
of this species can be calculated as 6+8+3=17, placing it in the middle portion of the high vulnerability category. Its conservation
status has not been evaluated by IUCN, and this species is not listed by SEMARNAT. Photo by Uri Garcta-Vdzque:.
*
=
7-3 4 ae ~~? :
and Solis in extreme western Coahuila” (Lemos-Espinal et al. 2015: 173). This individual was encountered at ca. 8 km SW from the
locality of San Antonio del Coyote, in the municipality of Matamoros. Wilson et al. (2013a) determined its EVS as 16, placing it in
the middle portion of the high vulnerability category. Its conservation status has been evaluated as Endangered by IUCN, but it has
not been listed by SEMARNAT. Photo by Marco Antonio Bazan-Tellez.
Amphib. Reptile Conserv. 44 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
oe a aa
: * pita fn
= Pane
by Daniel Garza-
Fig. 8. Serranias del Burro. Panoramic view of the Serranias del Burro, in the municipality of Zaragoza. Photo
Tobon.
138 genera of squamates in Mexico, the 44 represented Ambystoma velasci. Although Lemos-Espinal and Smith
in Coahuila amount to 31.9%. The six turtle genera (2016) reported A. mavortium in Coahuila, we consider
comprise 33.3% of the 18 genera with representatives in populations of Ambystoma in southeastern Coahuila to
Mexico. The total of 66 genera encompasses 30.6% of — belong to the same species that occurs in nearby Nuevo
the 216 found in Mexico (Johnson et al. 2017). Leon, which was identified as A. velasci by Nevarez-de
los Reyes et al. (2016).
Species
Gerrhonotus mccoyi. Recently, Garcia-Vazquez et al.
The herpetofauna of Coahuila represents 143 species, (2018) described this species from the Cuatro Ciénegas
including 20 anurans, four salamanders, 106 squamates, — Basin in the Sierras y Llanuras Coahuilenses region.
and 13 turtles (Table 3). The 20 anuran species comprise
8.1% of the 247 distributed in Mexico. The four Gerrhonotus parvus. Until recently, this species was
salamander species constitute 2.6% of the 151 found in —_ considered endemic to Nuevo Leon (Lemos-Espinal et
Mexico. The 106 squamate species make up 12.3% ofthe al. 2016). Banda-Leal et al. (2018), however, reported
863 located in Mexico. The 13 turtle species amount to it from Sierra de Zapalinamé, Coahuila. Therefore,
25.5% of the 51 species occurring in Mexico. The total — this species presumably has a continuous distribution
of 143 species comprises 10.8% of the 1,318 species throughout the Gran Sierra Plegada region between
making up the Mexican herpetofauna (Johnson, unpub.). —' the type locality (Galeana, Nuevo Leon) and Sierra
Zapalinameé, Coahuila.
Comments on the Species List
Sceloporus bimaculosus. A former subspecies of S.
Some comments on our list of recognized species are = magister (elevated by Schulte et al. 2006) was returned
necessary, especially as compared to that in Lemos- to the synonymy of S. magister by Leaché and Mulcahy
Espinal and Smith (2016), as follows: (2007). Curiously, a few sources since then (including
Lemos-Espinal and Smith’s (2016) most recent checklist
Eleutherodactylus marnockii. Although Lemos-Espinal on the herpetofauna of Coahuila and the Reptile Database
and Smith (2016) listed this frog as aresident of Coahuila, — website) referenced the former publication and continued
they provided no evidence based on voucher specimens. _ to recognize S. bimaculosus as a full species despite a short
In addition, neither Dodd (2013) nor Frost (2018) list this discussion of that issue by Wilson et al. (2015). In any event,
species as occurring 1n Mexico. Thus, we do not include _at this point, we herein recognize S. magister as the species
this species in our analysis.
Amphib. Reptile Conserv. 45 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
of the S. magister species group occurring in Coahuila.
Sceloporus cowlesi. Lemos-Espinal and Smith (2016) in
their recent checklist reported Sceloporus consobrinus
for the Coahuila herpetofauna. In a study of the molecular
phylogenetics of the Sceloporus undulatus species
group, however, Leaché (2009) restricted the distribution
of S. consobrinus to the United States and indicated the
member of the wndulatus group found within Nuevo
Leon to be S. cowlesi, which is the name we use here for
the Coahuilan populations.
Sceloporus gadsdeni. Diaz-Cardenas et al. (2017)
recently described this species from Sierra de San
Lorenzo, near Torreon, in the Bolson de Mapimi region.
Sceloporus ornatus. Herein we regard Sceloporus
oberon as a synonym of Sceloporus ornatus, based on
Martinez-Méndez and Méndez-de la Cruz (2007).
Sceloporus marmoratus. Unlike Lemos-Espinal and
Smith (2016), we do not list S. variabilis as occurring in
Coahuila, but based on Mendoza-Quiyano et al. (1998)
we do recognize S. marmoratus as occurring in the
Llanuras de Coahuila y Nuevo Leon region of Coahuila,
instead of S. variabilis.
Lampropeltis annulata. Lampropeltis annulata was
considered an evolutionary species separate from L.
triangulum by Ruane et al. (2014), who elevated a
number of subspecies of L. triangulum to full species
and synonymized others. Subspecies synonymized with
L. annulata included L. t. dixoni.
Lampropeltis gentilis. The first record for this species
from Mexico and Coahuila was reported by Baeza-Tarin
et al. (2018a).
Lampropeltis splendida. Lampropeltis splendida was
elevated to a full species separate from L. getula by
Pyron and Burbrink (2009).
Salvadora deserticola. Nevarez de los Reyes et al. (2018)
first reported this species from Coahuila.
Tantilla cucullata. Baeza-Tarin et al. (2018b) first
reported this species for Coahuila.
Trimorphodon vilkinsonii. Baeza-Tarin et al. (2018c)
first reported this species for Coahuila.
Crotalus ornatus. Anderson and Greenbaum (2012)
resurrected Crotalus ornatus from the synonymy of
C. molossus. Crotalus ornatus is found in most parts
of Coahuila, whereas C. molossus is restricted to the
extreme southern parts of the state.
Amphib. Reptile Conserv.
Apalone atra. Apalone atra has been either regarded as a
subspecies of A. spinifera or as a species endemic to the
Valley of Cuatro Ciénegas, where A. spinifera has gained
access to some areas through irrigation channels, thereby
allowing some genetic introgression to take place, and
driving A. atra to a level of being critically susceptible
to extinction. Smith and Smith (1979) had already
considered A. atra to be extinct. Recently, however, pure
individuals of A. atra have been found, as well as hybrids
between the two species (Cerda-Ardura et al. 2008).
See Wilson and Johnson (2010) for a discussion on this
issue. Until updated data indicate otherwise, we regard
A. atra as having viable populations in the Valley of
Cuatro Ciénegas, highlighting its need for conservation
assessment and action.
Patterns of Physiographic Distribution
Herein 10 physiographic regions are recognized in
Coahuila (Fig. 1), and the occurrence of the members of
the herpetofauna among these 10 regions are shown in
Table 4 and summarized in Table 5.
The total number of species in each region ranges
from a low of 38 in the Laguna de Mayran to a high
of 91 in the Sierras y Llanuras Coahuilenses (Table
5). The number of species in each of the other regions
is as follows, in ascending order: 40 (Sierra de la
Paila); 44 (Llanuras y Sierras Volcanicas); 45 (Bolson
de Mapimi); 45 (Serranias del Burro); 47 (Sierra
Transversales); 49 (Pliegues Saltillo Parras); 51 (Gran
Sierra Plegada); and 53 (Llanuras de Coahuila y Nuevo
Leon). The lowest value of 38 in the Laguna de Mayran
is 41.8% of the highest value of 91 in the Sierras y
Llanuras Coahuilenses. The latter region is the largest
in the state, but the former region is not the smallest (the
smallest region is the Gran Sierra Plegada).
As expected, the largest absolute and relative numbers
of the component herpetofaunal groups are found in the
Sierras y Llanuras Coahuilenses, including 14 of 24
species of amphibians (58.3%), 68 of 106 species of
squamates (64.2%), and nine of 13 species of turtles
(69.2%).
Members of the Coahuilan herpetofauna inhabit from
one to all 10 of the 10 physiographic regions, as follows:
one (66 of 143 species: 46.2%); two (25; 17.5%); three
(11; 7.7%); four (five; 3.5%); five (0; 0%); six (0; 0%);
seven (two; 1.4%); eight (five; 3.5%); nine (11; 7.7%);
and 10 (18; 12.6%). The most broadly distributed species
(occupying all 10 regions) are the anurans Anaxyrus
debilis, A. punctatus, Lithobates berlandieri, Scaphiopus
couchii, and Spea multiplicata;, the lizards Crotaphytus
collaris, Coleonyx brevis, Hemidactylus turcicus (non-
native), Phrynosoma cornutum, Sceloporus grammicus,
S. poinsetti, and Aspidoscelis gularis, and the snakes
Lampropeltis splendida, Masticophis flagellum,
Pantherophis emoryi, Pituophis catenifer, Rhinocheilus
lecontei, and Thamnophis marcianus. Given that Coahuila
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 4. Distribution of the amphibians, squamates, and turtles of Coahuila, Mexico, by physiographic region. Abbreviations are as
follows: BDM = Bolson de Mapimi; LSV = Llanuras y Sierras Volcanicas; LDM = Laguna de Mayran; SLC = Sierras y Llanuras
Coahuilenses; SDB = Serranias del Burro; SLP = Sierra de la Paila; PSP = Pliegues Saltillo Parras; STR = Sierras Transversales;
GSP = Gran Sierra Plegada; and LCN = Llanuras de Coahuila y Nuevo Leon. * = species endemic to Mexico; ** = species endemic
to Coahuila; and *** = non-native species. See text for detailed descriptions of these regions.
Physiographic Regions of Coahuila Number
Taxa of Regions
| Bufonidae(7speciesy | | EE
ee ee a a
Anasymis debits a oe eae ae ee io |
ce a i Co
ee a a (i ee QR a a
| Anaxyruswoodhousii_ | + OL + TT
| Rhinellahorribilis | Et TE
| Craugastoridae(I species) | | EE
| Craugastoraugusti | Tt
| Eleutherodactylidae(3speciesy) | | | TT
| Eleutherodactylus cystignathoides_ | |_| ST ST CE TE
| Eleutherodactylus gutilatus | | TE + TOE CE vt TT
| Eleutherodactyluslongipes* | | ST TE Et Tt |
| Hylidae(4speciesy | |
| Acris blanchardi TT tT
| Dryophytesarenicolor | TE Et TCE
| Rheohylamiotympanum® | LE
| Smiliscabaudinii | Et
| Microhylidae(1 species) | | TE
| Gastrophryne olivacea | + | + | + [| + | + P+] + To + | +t TT
| Ranidae(2speciesy) | |
| Lithobates catesbeianus*** | + [Tt Tt 8
| Scaphiopodidae(2 species) | | | EE
| Caudata(4speciesy |
| Ambystomatidae(I species) | | | TE EE
| Ambystomavelasci* | TE Et
| Plethodontidae(3speciesy | | TE EE
| Aquiloewryceagaleanae* | TT tT
| Aquiloeurycea scandens* | TT tT
| Chiropterotritonpriscus* | TE tT
| Squamata(106 species) | | TE
| Anguidae(Sspeciesy | | TE
Be ee i a a ee ee ee eee ee
| Gerrhonotusinfornalis, | ee eee +t ee
| Gerrhonostugoi** | Tt
| Gerrhonotusmecoyi** | Tt TE
| Gerrhonotusparvus* | TE
| Crotaphytidae(4 species) | |
| Crotaphytusantiquis** | Tt
| Crotaphytusreticulatus | LE
| Gambeliawistizeni | Lt TE
| Eublepharidae(2species) | | | CE
| Coleonyxreticulas | Tt TE
| Gekkonidae(I species) | | EC CC CE
Amphib. Reptile Conserv. 47 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 4 (continued). Distribution of the amphibians, squamates, and turtles of Coahuila, Mexico, by physiographic region.
Abbreviations are as follows: BDM = Bolson de Mapimi; LSV = Llanuras y Sierras Volcanicas; LDM = Laguna de Mayran; SLC =
Sierras y Llanuras Coahuilenses; SDB = Serranias del Burro; SLP = Sierra de la Paila; PSP = Pliegues Saltillo Parras; STR = Sierras
Transversales; GSP = Gran Sierra Plegada; and LCN = Llanuras de Coahuila y Nuevo Leon. * = species endemic to Mexico; ** =
Species endemic to Coahuila; and *** = non-native species. See text for detailed descriptions of these regions.
Physiographic Regions of Coahuila Number
Taxa of Regions
[Phrynosomatidae @9 species) |_| _ =r
ee ee SS
| Holbrookia approximans* |_| + | + | + | + [+ }]+] +] + | | 9 |
| Holbrookialacerata | | | CCT CCT CT Cs Tt
| Phrynosoma modestum ss |_+ | + | + | + | + [+] +] +] + | | 9 |
| Phrynosoma orbicuare* |_| | | CCE CT CT +t T+ TCU
| Sceloporuscautus* | tT TT CT CT
| Sceloporuscouchii* | | dT dE + TUT + T+ T+} TUT
[| Sceloporuscowlesi | + | + | + | + | + f+ t+] +] + | [| 9 |
| Sceloporuscyanogenys |_| | dT + | UT CT
| Sceloporuscyanosticius* |_| | CT CT CT C+ T+ TUT
| Sceloporusgadsdeni** | + | LT dT CT CT
| Sceloporusgoldmani* | | | CT CCT CT CT Tt
| Sceloporus grammicus | + | + | + | + | + |+ | +] +] + | + | 0
| Sceloporusmaculosus* | + | | | CT CT CT + Tk
[| Sceloporusmagister | | *# [| TE + | oT + TUT CUT CCU
| Sceloporusmarmoraus {|_| | | CCE CT CT
[| Sceloporusmerriami | tT dT dE + TOUT + | + Ts |
| Sceloporusminor* | tT TT CT CT
| Sceloporusolivaceus | | | dT + T+ TUT CU
| Sceloporusornatus* | TT TE CT CT CT} TU
| Sceloporusparvus* | tT TE TO
| Sceloporuspoinsetii | + | + | + | + | + P+ t+ P+ | + | + |
| Sceloporussamcolemani* |_| | dT CT CT CT Tt
A EO ee
Uma exsul**
a a | a! a a a a (ar ay
| Urosaurusornaus | + TL dE +hT + TUT
| Uta stansburiana | +} TE + | +! T+ |] T+ T+ T+! T+! TUT 8
| Scincidae(3speciesy | | | | CT CT CT
| Plestiodondicei* | | CT CT CT CT
| Plestiodon obsolems | + | + | + | + | + | +> +] +] t+] 9 |
| Plestiodon tetragrammus {|_| | dL + T+ TUT CU
| Sphenomorphidae(3 species) {|__| | S| CT CT CT
| Scincellakikaapoa** | | dT Cd + TUT CT
| Scincellalateralis | | CT CE + TUT CT
| Scincellasivicola* | | dT CL CCT CT Tt
| Teiidae(4speciesy | | CT CT CCT CC
| Aspidoscelis gularis | + | + | + | + | + |+ | +] +] + | + | 0 |
| Aspidoscelis inornata | + | + | + | + | + |+ t+] +] + | | 9
| Aspidoscelis marmorata | _ + | + | + | + | + [+ t]+t] +t] | | 8 |
| Aspidoscelis tesselaa | | + | | + | tT TC
| Xantusiidae(I species) |_| | | CE CT CT
| Xantusiaextorris* | ET
| Colubridae(29speciesy | | CE | CE CE
| Arizonaelegans | +} Tc *® | +! T+ T+ t+ P+] oT hut +h TL 8
| Bogertophis subocularis | + | + | + | + | + [+ ]+] | | | 7 |
| Coluber conswrictor | dT dT CT + TUT CT CO
NPENTNP Re fee _wepTy
nn
Amphib. Reptile Conserv. 48 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 4 (continued). Distribution of the amphibians, squamates, and turtles of Coahuila, Mexico, by physiographic region.
Abbreviations are as follows: BDM = Bolson de Mapimi; LSV = Llanuras y Sierras Volcanicas; LDM = Laguna de Mayran; SLC =
Sierras y Llanuras Coahuilenses; SDB = Serranias del Burro; SLP = Sierra de la Paila; PSP = Pliegues Saltillo Parras; STR = Sierras
Transversales; GSP = Gran Sierra Plegada; and LCN = Llanuras de Coahuila y Nuevo Leon. * = species endemic to Mexico; ** =
Species endemic to Coahuila; and *** = non-native species. See text for detailed descriptions of these regions.
Physiographic Regions of Coahuila Number
Taxa of Regions
LCN Occupied
LDM T
~
Lampropeltis annulata
Lampropeltis gentilis
Lampropeltis leonis*
Lampropeltis splendida
—
-)
Masticophis flagellum
Masticophis schotti
Masticophis taeniatus
Opheodrys aestivus
Pantherophis bairdi
—
co)
Pantherophis emoryi
—
>)
Pituophis catenifer
Pituophis deppei*
—
>)
Rhinocheilus lecontei
Salvadora deserticola
Salvadora grahamiae
Sonora episcopa
Tantilla atriceps
Tantilla cucullata
Tantilla gracilis
Tantilla hobartsmithi
Tantilla nigriceps
Tantilla wilcoxi
Trimorphodon vilkinsonii
Dipsadidae (4 species)
Diadophis punctatus
Heterodon kennerlyi
Hypsiglena jani
Leptodeira septentrionalis
Elapidae (1 species)
Micrurus tener
Leptotyphlopidae (3 species)
Rena dissecta
Rena dulcis
Rena segrega
Natricidae (7 species)
Nerodia erythrogaster
Nerodia rhombifer
Storeria hidalgoensis*
Thamnophis cyrtopsis
Thamnophis exsul*
Thamnophis marcianus
Thamnophis proximus
DN
+) 4+]+ + |+ + + +/+ ]+ + ee iat [ete + +] +/+ + +/+) +) +] + +/+ areal |
DN
+] + + + +] +] + + + +] + +] + =
DN
+ + +] + + + +] + +|+ oe
ine]
in|
+] + + +])4+]+ + + + +] + +|+ + w
Dn
+ + + +] + + +/+]/+]+ +|+
Crotalus molossus
Amphib. Reptile Conserv. 49 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 4 (continued). Distribution of the amphibians, squamates, and turtles of Coahuila, Mexico, by physiographic region.
Abbreviations are as follows: BDM = Bolson de Mapimi; LS V = Llanuras y Sierras Volcanicas; LDM = Laguna de Mayran; SLC =
Sierras y Llanuras Coahuilenses; SDB = Serranias del Burro; SLP = Sierra de la Paila; PSP = Pliegues Saltillo Parras; STR = Sierras
Transversales; GSP = Gran Sierra Plegada; and LCN = Llanuras de Coahuila y Nuevo Leon. * = species endemic to Mexico; ** =
Species endemic to Coahuila; and *** = non-native species. See text for detailed descriptions of these regions.
Physiographic Regions of Coahuila
Taxa
Crotalus pricei
Crotalus scutulatus
Crotalus viridis
Sistrurus tergeminus
Testudines (13 species)
Emydidae (6 species)
Pseudemys gorzugi
Terrapene coahuila**
Terrapene ornata
Trachemys gaigeae
Trachemys scripta***
Trachemys taylori**
Kinosternidae (3 species)
Kinosternon durangoense*
Kinosternon flavescens
Kinosternon hirtipes
Testudinidae (2 species)
Gopherus berlandieri
Apalone spinifera
borders the US state of Texas, it is not surprising that
all 18 of these species, including the introduced species
Hemidactylus turcicus, also are distributed in the USA.
Of the 143 species comprising the Coahuilan
herpetofauna, 91 (63.6%) are found in only one or two
physiographic regions, which is of great conservation
significance (see below). The mean regional occupancy
is 3.5.
Single-region species: Limited distribution increases
conservation concern. The number of species found ina
single region varies from one (in the Laguna de Mayran,
Llanuras y Sierras Volcanicas, and Pliegues Saltillo-
Parras) to 23 (in the Sierras y Llanurus Coahuilenses). No
single-region species are found in the Serranias del Burro
region. On the following lists, * = endemic to Mexico,
but found in more than one state; and ** = endemic to
Coahuila.
Of the 23 single-region species in the Sierras y
Llanuras Coahuilenses listed here by taxonomic order, 17
are Mexican non-endemics and the other six are endemic
only within the boundaries of Coahuila.
Craugastor augusti
Dryophytes arenicolor
Gerrhonotus lugoi**
Amphib. Reptile Conserv.
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Gerrhonotus mccoyi**
Gambelia wislizenii
Coleonyx reticulatus
Scincella kikaapoa**
Scincella lateralis
Coluber constrictor
Opheodrys aestivus
Pantherophis bairdi
Salvadora grahamiae
Tantilla atriceps
Tantilla hobartsmithi
Leptodeira septentrionalis
Rena dissecta
Thamnophis cyrtopsis
Crotalus ornatus
Crotalus viridis
Sistrurus tergeminus
Terrapene coahuila**
Trachemys taylori**
Apalone atra**
Of the 15 single-region species in the Gran Sierra
Plegada listed here, 13 are country endemics and the
other two are Mexican non-endemics.
Rheohyla miotympanum*
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
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October 2019 | Volume 13 | Number 2 | e189
51
Amphib. Reptile Conserv.
The herpetofauna of Coahuila, Mexico
Smilisca baudinii
Aquiloeurycea galeanae*
Aquiloeurycea scandens*
Chiropterotriton priscus*
Barisia imbricata*
Gerrhonotus parvus*
Sceloporus minor*
Plestiodon dicei*
Scincella silvicola*
Lampropeltis leonis*
Storeria hidalgoensis*
Thamnophis exsul*
Crotalus morulus*
Crotalus pricei
All of the 12 single-region species in the Llanuras de
Coahuila y Nuevo Leon listed here are non-endemic to
Mexico:
Eleutherodactylus cystignathoides
Acris blanchardi
Crotaphytus reticulatus
Holbrookia lacerata
Sceloporus marmoratus
Masticophis schotti
Salvadora deserticola
Tantilla cucullata
Tantilla gracilis
Tantilla nigriceps
Trimorphodon vilkinsonii
Nerodia rhombifer
Six of the seven single-region species in the Sierras
Transversales listed here are country endemics and the
other is a non-endemic:
Ambystoma velasci*
Sceloporus cautus*
Sceloporus goldmani*
Sceloporus samcolemani*
Sceloporus spinosus*
Xantusia extorris*
Kinosternon hirtipes
Three of the five single-region species in the Bolson
de Mapimi are country endemics, and the other two are
state endemics:
Sceloporus gadsdeni**
Uma exsul**
Uma paraphygas*
Kinosternon durangoense*
Gopherus flavomarginatus*
The single-region species in the Laguna de Mayran is
a state endemic lizard:
Amphib. Reptile Conserv.
52
Crotaphytus antiquus
The one single-region species in the Llanuras y Sierras
Volcanicas is a non-endemic turtle:
Terrapene ornata
The one single-region species in the Pliegues Saltillo-
Parras is a non-endemic snake:
Tantilla wilcoxi
Examination of the above-listed species indicates that
of the 65 single-region species in Coahuila, 22 are country
endemics and nine are state endemics. The remaining 34
are non-endemic species that are also distributed in the
USA.
Coefficient of Biogeographic Resemblance. A
Coefficient of Biogeographic Resemblance (CBR)
matrix was created for examining herpetofaunal
relationships among the 10 physiographic regions of
Coahuila (Table 6) and these data were used to produce a
UPGMA dendrogram (Fig. 12). As mentioned above, the
numbers of species within the 10 physiographic regions
of Coahuila range from a high of 91 species within the
Sierras y Llanuras Coahuilenses (SLC) to a low of 38
within Laguna de Mayran (LDM). The mean species
richness number for all 10 regions is 50.3. The numbers
of species shared between regions range from 20 to 45.
The lowest value of 20 is found between only one pair of
regions, the Llanuras de Coahuila y Nuevo Leon (LCN)
and Gran Sierra Plegada (GSP). The highest number is
also shared between only one pair of regions, the SLC
and Serranias del Burro (SDB). The mean number of
shared species among the 45 regional pairings 1s 32.9.
The lowest number of 20 shared species between LCN
and GSP makes biogeographic sense because these two
regions are situated at opposite ends of the state, are not
connected geographically, and are environmentally quite
different: LCN contains subhumid lowland plains and
hills versus GSP with semihumid to subhumid highland
mountainous areas carved by deep valleys. Also, GSP has
a much smaller area in Coahuila than does LCN. On the
other hand, the two regions with the highest number of
AS shared species are SLC and SDB. These two regions
share part of their borders and both contain similar
ecological regimes. Unlike the situation in Tamaulipas
(Teran-Juarez et al. 2016), the higher numbers of species
in the regional pairings in Coahuila, with the exception
of SLC (91 species), do not necessarily equate to higher
numbers of shared species, which is more similar to the
patterns shown in adjacent Nuevo Leon (Navarez-de
los Reyes et al. 2016). This discrepancy is most likely
due to the larger number of included physiographic
regions, and the lower number of shared species from
more distant regions. Reflecting this trend, the following
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 6. Pair-wise comparison matrix of Coefficient of Biogeographic Resemblance (CBR) data of herpetofaunal relationships for
the 10 physiographic regions in Coahuila, Mexico. Underlined values = number of species in each region; upper triangular matrix
values = species in common between two regions; and lower triangular matrix values = CBR values. The formula for this algorithm
is CBR = 2C/N, + N, (Duellman 1990), where C is the number of species in common to both regions, N, is the number of species
in the first region, and N, is the number of species in the second region. See Table 4 for explanation of abbreviations and Fig. 12 for
the UPGMA dendrogram produced from the CBR data.
BDM LSV LDM SLC
BDM 45 38 af 38
LSV 0.85 44 37 42
LDM 0.89 0.90 33 ey
SLC 0.56 0.62 0.57 91
SDB 0.76 0.81 0.82 0.66
SLP 0.85 0.88 0.92 0.61
PSP 0.79 0.80 0.83 0.63
STR 0.72 0.70 0.75 0.49
GSP 0.60 0.61 0.65 0.44
LCN 0.45 0.45 0.48 0.56
SDB SLP PSP STR GSP LCN
34 36 37 33 29 22
36 37 36 32 29 22
34 36 36 32 I) 22
45 40 4 34 31 40
45 35 37 30 27 28
0.74 40 38 34 29 24
0.79 0.85 49 35 32 24
0.65 0.78 0773 47 31 21
0.56 0.64 0.64 0.63 Si 20
0.57 0.52 0.47 0.42 0.38 53
pairwise comparisons of regions are aligned in order of
highest to lowest species richness (underlined values)
and their corresponding numbers of shared species (in
parentheses) with all other regions; see text and map for
discussions on characteristics and sizes of the regions:
SLC 91: SDB (45), SLP (40), PSP (44), STR (34),
GSP (31), LCN (40), LDM (32), LSV (42), BDM (38).
LCN 53: GSP (20), STR (21), PSP (24), SLP (24),
SDB (28), SLC (40), LDM (22), LSV (23), BDM (22).
GSP 51: LCN (20), STR (31), PSP (32), SLP (29),
SDB (27), SLC (31), LDM (29), LSV (29), BDM (29).
PSP 49: STR (35), GSP (32), LCN (24), SLP (38),
SDB (37), SLC (44), LDM (36), LSV (36), BDM (37).
STR 47: GSP (31), LCN (21), PSP (35), SLP (34),
SDB (30), SLC (34), LDM (32), LSV (32), BDM (33).
SDB 45: SLP (35), PSP (27), STR (30), GSP (27), LCN
(28); SLC (45), LDM (34), LSV (36), BDM (34).
BDM 45: LSV (38), LDM (37), SLC (38), SDB (34),
SLP (36), PSP (37), STR (33), GSP (29), LCN (22).
LSV 44: BDM (38), LDM (37), SLC (42), SDB (36),
SLP (37), PSP (36), STR (32), GSP (29), LCN (22).
SLP 40: BDM (36), LSV (37), LDM (36), SLC (40),
SDB (35), PSP (38), STR (34), GSP (29), LCN (24).
LDM 38: BDM (37), SLP (36), PSP (36), STR (32),
GSP (29), LCN (22), SLC (37), SDB (34), LSV (34).
SLC, with its 91 species, is the largest physiographic
region in Coahuila that shares borders to variable extents
with five of the nine other regions in the state (LCN,
SDB, PSP, LSV, SLP), including the 2™ and 4" most
speciose regions (LCN, PSP). The 91 species in SLC
reveals a large discrepancy between it and all nine other
regions in the state. Ninety-one species is 38 more than
found in LCN, the second most species-rich region with
53 species, whereas the total difference for all nine of the
Amphib. Reptile Conserv.
other regions is only 15 species between the 53 species in
LCN and the 38 species in LDM. LCN is a lowland region
next to the Rio Grande with few montane landscapes, but
it contains several generalist herpetofaunal species that
also exist in adjacent montane regions of Coahuila at
lower elevations. PSP is mostly separated from LCN by
two other regions to its north (LDM, SLP); however, it
shares a geographic connection through a northwestern
extension of PSP in Nuevo Leon (Nevarez-de los Reyes
et al. 2016).
The following data show ranges and mean numbers
of shared species for each of the 10 regions listed above
that are arranged according to increasing mean numbers
(bold in parentheses) with underlined values referring to
species richness in each region:
Llanuras de Coahuila y Nuevo Leon (LCN) (53): 20-—
40 (24.7)
Gran Sierra Plegada - GSP (51): 20-32 (28.5)
Sierras Transversales - STR (47): 21-35 (31.3)
Laguna de Mayran - LGM (38): 22-37 (33.3)
Bolson de Mapimi - BDM (45): 22—38 (33.8)
Serranias del Burro - SDB (45): 27-45 (34.0)
Llanuras y Sierras Volcanicas - LSV (44): 22-42 (34.3)
Sierra de la Paila - SLP (40): 2440 (34.3)
Pliegues de Saltillo Parras - PSP (49): 24-38 (35.4)
Sierras y Llanuras Coahuilenses - SLC (91): 31-45 (39.0)
With the exception of SLC and PSP (1* and 4" highest
in species richness, and 1%‘ and 2" highest mean numbers
of shared species, respectively), the mean number of
pairwise species comparisons between all other regions
indicate that higher species richness in a region does not
necessarily translate into a higher mean number of shared
species when all regions are totaled. Apparent extreme
examples of this are: LCN, GSP, and STR, respectively,
having the 1%, 2" and 3™ highest numbers of species
and lowest mean numbers of shared species. It makes
sense that LCN would share fewer species with other
regions in Coahuila because of its ecological uniqueness
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Fig. 9. Sierras y Llanuras Coahuilenses. Vegetation in the Val-
ley of Cuatrociénegas, in the municipality of Cuatrociénegas de
Carranza. Photo by Eli Garcia-Padilla.
Fig. 11. Sierras Transversales. Paso de Carneros, Matorral ro-
setophilous vegetation, with Chocha (Yucca carnerosana) and
Lechuguilla (Agave lechuguilla), at Paso de Carneros, in the
municipality of Saltillo. Photo by Manuel Nevarez de los Reyes.
associated with lower elevations and general differences
in vegetation formations and topography, as well as
herpetofaunal affinities to the United States northward
across the Rio Grande. GSP has the smallest area of all
regions in the state, but is much more extensive when
considering it also exists in Nuevo Leon and Tamaulipas
(Nevarez-de los Reyes et al. 2016; Teran-Juarez et al.
2016). STR is a slender montane region with high species
richness positioned primarily within Coahuila across its
entire southern border.
UPGMA Dendrogram. Based on the data in Table 6, a
UPGMA dendrogram (Fig. 12) was created to illustrate
the herpetofaunal resemblance patterns in a hierarchical
fashion among the 10 physiographic regions of Coahuila
(Fig. 1). The patterns are different when compared to
those shown in the two other northern Mexico states
bordering Texas that were covered in previous MCS
publications: Nuevo Leon (Nevarez-de los Reyes et al.
2016) and Tamaulipas (Teran-Juarez et al. 2016). The
Coahuila dendrogram shows the similarity relationships
in descending order from the most similar regions,
SLP clustering with LDM at a value of 0.92, down to
the lowest value, where LCN clusters with all the other
regions at a value of 0.48. In other words, there are no
Amphib. Reptile Conserv.
Fig. 10. Sierra de la Paila. Vegetation in the Sierra de la Paila,
in the municipality of Ramos Arizpe. Photo by Bernardo Ma-
rino (http://gransierraplegada.org).
distinct subgroupings within the dendrogram, which
indicates on a biogeographic scale that there are no
distinct subgroups composed of distributional units that
share more closely related herpetofaunas. On the other
hand, neighboring Nuevo Leon with seven regions
has two distinct biogeographic subgroups, a southern
unit containing two regions and a more northern unit
containing five regions that clusters with the southern
unit at the 0.37 similarity level. Tamaulipas, also with
seven recognized regions, has the most complex pattern
of herpetological similarity of these three states. Two
biogeographic subgroups are found in what can be
considered the northern and eastern sections of the
state. One of those subgroups contains three regions that
make up the majority of the state’s area, while the other
subgroup is comprised of two small disjunct highland
regions that cluster together at the 0.55 level; and both
are nested within one of the other subgroup’s regions.
Those two subgroups cluster with each other at the 0.46
similarity level. One of the two remaining regions, which
make up the extreme southwestern sector of Tamaulipas,
clusters independently with the other two biogeographic
subgroups at the 0.44 level of herpetofaunal similarity.
The last region, which is the southwestern-most
section of the state, 1s the most distinctive of the seven,
thereby clustering with the others at the 0.23 level of
herpetological similarity.
In summary, the UPMGA dendrogram for Coahuila
shows that the lowland non-montane region (LCN)
bordering the Rio Grande and Texas is the most
distinctive region in Coahuila as far as herpetological
similarity goes, based on numbers of shared species.
It also shows a pattern of similarity among regions in
close proximity to each other that also share ecological
parameters either within the state or through areas of the
same physiographic region outside Coahuila.
Distribution Status Categorizations
The discussion of the distribution status of Coahuilan
herpetofauna members uses the system developed by
Alvarado-Diaz et al. (2013), and employed in all the
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
SLC GSP
LCN STR SDB
PSP
BDM LSV SLP LDM
Fig. 12. AUPGMA generated dendrogram illustrating the similarity relationships of species richness among the herpetofauna in the
10 physiographic regions of Coahuila (based on the data in Table 6). We calculated the similarity values using Duellman’s (1990)
Coefficient of Biogeographic Resemblance (CBR).
other entries in the Mexican Conservation Series. The
categories in the system are non-endemic, country
endemic, state endemic, and non-native (Tables 7 and 8).
Given the 512-km-long border shared between
Coahuila and Texas (http://wikipedia.org; accessed
11 August 2018), it is not surprising that the largest
component of the herpetofauna falls into the non-
endemic category. Of the 143 species comprising the
Coahuilan herpetofauna, 100 species (69.9% of the total)
belong to this category. Almost half (49) of the non-
endemic species are snakes, and this number is only five
fewer than the total number of snake species in the entire
herpetofauna (Table 8). The 76 non-endemic squamate
species are 71.7% of the total of 106 species for the state.
In addition, a large portion of the state’s anurans (17 of
20; 85.0%) are also non-endemic species. On the other
hand, slightly more than half the turtle species (seven of
13; 53.8%) are non-endemic to Coahuila (Table 8).
The next largest component is the 31 (21.7%) country
endemic species, most of which are squamates, including
18 lizards and five snakes (74.2%). The remainder
are amphibians (six species; 19.4%) and turtles (two
species; 6.5%). Almost half of the country endemics are
phrynosomatid lizards (14 of 31; 45.2%).
Only nine of the species (6.3%) in Coahuila are state
endemics. Six of these are lizards (Gerrhonotus lugoi,
G. mccoyi, Crotaphytus antiquus, Sceloporus gadsdeni,
Uma exsul, and Scincella kikaapoa) and three are turtles
(Terrapene coahuila, Trachemys taylori, and Apalone
atra).
The number of non-native species in Coahuila is
only three, the ranid frog Lithobates catesbeianus, the
Amphib. Reptile Conserv.
gekkonid lizard Hemidactylus turcicus, and the emydid
turtle Trachemys scripta. These three species also were
reported as introduced into Nuevo Leon (Nevarez-de los
Reyes et al. 2016).
The number of endemic species in Coahuila (country
and state endemics combined) is 40, which is 4.9% of
the total number of endemic species for Mexico (811;
Johnson unpub.). The number of non-endemic species is
100, which is 19.7% of the total of such species in the
entirety of Mexico (508; Johnson unpub. ).
Principal Environmental Threats
In this section we examine the 12 problems we think are
the most significant in affecting the sustainability of the
populations of Coahuila’s amphibians and reptiles.
Urban development. As of 2015, the population of
Coahuila was 2,954,915, making it the 16" most densely
populated state in Mexico. The Municipality of Saltillo is
the most populated of the 38 municipalities in the state,
with a population of 807,537 people, followed by the
municipalities of Torredn with 679,288, Monclova with
231,107, and Piedras Negras with 163,595 (see INEGI,
http://www. beta.inegi.org.mx/temas/estructura/). Data
from this same website indicate that 90% of the state
population is located in urban areas, with the remainder
in rural areas. The current annual percentage growth
rate 1s 1.5%, which portends a doubling rate of about 47
years. Most of this growth is expected to occur within the
most heavily-populated municipalities.
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 7. Distributional and conservation status measures for members of the herpetofauna of Coahuila, Mexico. Distributional
Status: SE = endemic to state of Coahuila; CE = endemic to country of Mexico; NE = not endemic to state or country; and NN
= non-native. Environmental Vulnerability Score (taken from Wilson et al. 2013a,b): low (L) vulnerability species (EVS of 3-9);
medium (M) vulnerability species (EVS of 10—13); and high (H) vulnerability species (EVS of 14—20). IUCN Categorization: CR =
Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data Deficient; NE
= Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered; Pr = Special Protection; and NS = No Status. * = species
endemic to Mexico; ** = species endemic to Coahuila; *** = non-native species. See text for explanations of the EVS, IUCN, and
SEMARNAT rating systems.
Datributionale ||| oo ronmental IUCN SEMARNAT
Vulnerability aecid
Status Category (Score) Categorization Status
| Lithobates catesbeianus***_ | NNT OS
| Hemidactylus turcicus*** | NN
Amphib. Reptile Conserv. 56 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 7 (continued). Distributional and conservation status measures for members of the herpetofauna of Coahuila, Mexico.
Distributional Status: SE = endemic to state of Coahuila; CE = endemic to country of Mexico; NE = not endemic to state or country;
and NN = non-native. Environmental Vulnerability Score (taken from Wilson et al. 2013a,b): low (L) vulnerability species (EVS of
3-9); medium (M) vulnerability species (EVS of 10-13); and high (H) vulnerability species (EVS of 14—20). IUCN Categorization:
CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data
Deficient; NE = Not Evaluated. SEMARNAT Status: A= Threatened; P = Endangered; Pr = Special Protection; and NS = No Status.
* = species endemic to Mexico; ** = species endemic to Coahuila; *** = non-native species. See text for explanations of the EVS,
IUCN, and SEMARNAT rating systems.
Distributional || vironmental IUCN SEMARNAT
Vulnerability ae
Status Category (Score) Categorization Status
| Umaexsul** TSE HS) | ENT |
| Umaparaphygas* | CE) | NTP
Amphib. Reptile Conserv. 57 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 7 (continued). Distributional and conservation status measures for members of the herpetofauna of Coahuila, Mexico.
Distributional Status: SE = endemic to state of Coahuila; CE = endemic to country of Mexico; NE = not endemic to state or country;
and NN = non-native. Environmental Vulnerability Score (taken from Wilson et al. 2013a,b): low (L) vulnerability species (EVS of
3-9); medium (M) vulnerability species (EVS of 10—13); and high (H) vulnerability species (EVS of 14—20). IUCN Categorization:
CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data
Deficient; NE = Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered; Pr = Special Protection; and NS = No Status.
* = species endemic to Mexico; ** = species endemic to Coahuila; *** = non-native species. See text for explanations of the EVS,
IUCN, and SEMARNAT rating systems.
Taxa Status Sy HEE AUILY, Categorization Status
Category (Score) 8
| Trachemys scripta*** | NNT
| Kinosternon durangoense* | CCE OT CO) S|
Amphib. Reptile Conserv. 58 October 2019 | Volume 13 | Number 2 | e189
N Ls
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Lazcano et al.
Fig. 13. Urban Development. Urban growth near Saltillo,
reaching the limit of the Natural Protected Area “Sierra de
Zapalinamé,” in the municipality of Saltillo. Photo by Manuel
Nevarez de los Reyes.
eee oe ee
Fig. 15. Deforestation for Agricultural Purposes. Monoculture
of grapes near Parras de la Fuente, in the municipality of Parras.
Photo by Manuel Nevarez de los Reyes.
Urban pollution. One outcome of urban growth that
is of environmental significance is the accumulation of
garbage resulting from the inefficient use of resources
by populations in urban areas. An extensive recent study
acknowledged that “garbage is the major environmental
problem facing Mexico, involving the generation of more
than 100 million tons of wastes per year that are not
handled in an adequate manner” (http://www.estosdias.
com.mx/blog/archivos/226; accessed 18 September
2018). This site points out that the Federal District and
its metropolitan area has the largest garbage dump in the
world, located in Ciudad Nezahualcoyotl in the State of
México. The useful life of this site has been extended
despite the lack of additional space being available,
which points out the difficulty of finding other sites to
deposit the thousands of tons of garbage produced.
With reference to Coahuila, in an article published in
Torreon on 14 August 2018 by Noticias—El Sol de la
Laguna, the Secretary of the Environment, Eglantina
Canales Gutiérrez, reported that 3,000 tons of garbage
are produced in the state of Coahuila on a daily basis,
or almost one kilogram of trash produced per person
Amphib. Reptile Conserv.
Fig. 14. Industrial Pollution. Factories polluting the air in the
vicinity of Monclova, in the muncipality of Monclova. Photo
by Michael Price.
Fig. 16. Deforestation for Agricultural Purposes. Monocul-
ture of cotton at San Pedro de las Colonias, in the municipality
of the same name, Provincia de Laguna de Mayran. Photo by
Manuel Nevarez de los Reyes.
per day. Secretary Canales stated that the burial of such
trash in landfills, which are available in 85% of Coahuila,
represents the best solution to date, but that in the future
efforts to recycle products should be implemented. She
decried that often garbage does not end up tn landfills,
but rather is left out in the open. This environmental
problem can be expected to grow commensurate with the
rate of human population growth in Coahuila.
Several instances of the direct impact of accumulated
garbage on members of the Mexican herpetofauna have
been documented. Lazcano et al. (2006) reported the
death of several Texas Horned Lizards (Phrynosoma
cornutum), that were trapped inside a discarded tire in
an illegal dump site in the neighboring state of Nuevo
Leon. The lizards, presumably seeking shelter, died
after they were unable to escape due to the intense daily
temperatures at this locality that can rise to 45 °C in the
shade. On another occasion in Nuevo Leon, Chavez-
Cisneros et al. (2010) reported finding a Greater Earless
Lizard (Cophosaurus texanus) that apparently died after
ingesting a deflated balloon left in a pile of litter. The full
environmental impact of discarded trash on the native
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 8. Summary of the distributional status of herpetofaunal families in Coahuila, Mexico.
Distributional Status
Number of
Families ;
Species
Hylidae
Microhylidae
Ranidae
Scaphiopodidae
Subtotals
Plethodontidae
Sphenomorphidae
A
Teiidae i
Xantusiidae
4
Dipsadidae
Elapidae
Leptotyphlopidae
Natricidae
Viperidae
Subtotals
Emydidae
Kinosternidae
Sum Totals
herpetofauna of Coahuila, and elsewhere in Mexico, is
still unknown, so it 1s imperative that actions be taken to
diminish this overtly intentional behavior by an uncaring
populace.
Industrial pollution. The municipalities of Acufia,
Monclova, Piedras Negras, Ramos Arizpe, Saltillo, and
Torreon have a Vehicle Verification Program (PVV) to
address vehicular air pollution, which is supervised
under municipal authority (Anon 2017).
Coahuila produces 16% of the electric power and
23% of the steel in Mexico. The industry dedicated
to the extraction and commercialization of coal, in
the coal region around Nava and Piedras Negras, has
Amphib. Reptile Conserv.
Non-endemic
Country
Endemic
(CE)
State Non-native
Endemic (SE)
been named as the one that most intensively pollutes
the air (Journalistic note of May 4, 2016, http://www.
vanguardia.com.mx/articulo/empresas-carboneras-las-
que-mas-contaminan-el-aire-en-la-carbonifera-y-norte-
de-coahuila).
Deforestation for agricultural and ranching purposes.
One of the most notorious cases of massive deforestation
carried out in the state of Coahuila happened in 2001.
It occurred in the Valle del Hundido, adjacent to the
Cuatro Ciénegas Valley, where hundreds of hectares
were cleared for the establishment of alfalfa crops to
feed dairy and beef cattle (http://www.vanguardia.com.
mx/columnas-elhundido-1728357.html). Another case
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
== : 7 a ee | = ~ = ‘\ : —e a a
No. 9. Phrynosoma orbiculare (Linnaeus, 1758). The Mountain Horned Lizard is a Mexican endemic species that occurs “from
eastern Sonora and western Chihuahua southward through the mountains of Durango, Zacatecas, Aguascalientes, Jalisco, and
Michoacan, and from the mountains of southern Nuevo Leon southward through San Luis Potosi, Querétaro, Hidalgo, Veracruz,
and westward through Puebla, Tlaxcala, Mexico, the Distrito Federal, and Morelos” (Lemos-Espinal and Dixon 2013: 122). Bryson
et al. (2011) noted, however, that this species is probably comprised of several distinct lineages, of which some appear to have
small distributions and long independent evolutionary histories, and that some of these lineages merit additional consideration for
protection. This individual was found near Monterreal, in the municipality of Arteaga. Wilson et al. (2013a) calculated its EVS as
12, placing it in the upper half of the medium vulnerability category. Its conservation status has been reported as Least Concern by
IUCN, and as threatened (A) by SEMARNAT. Photo by Eli Garcia-Padilla.
~ Rat r o /. »
.- = fe tom a” ‘. = s Ae > * a
No. 10. Sceloporus cautus Smith, 1938. The Shy Spiny Lizard is an endemic Mexican lizard distributed from “the western slopes
of the Sierra Madre Oriental in Tamaulipas, southeastern Coahuila, and central Nuevo Leon southward through much of San Luis
Potosi and the northern half of Zacatecas” (Lemos-Espinal and Dixon 2013: 124). This individual was found at Cafion el Chorro, in
the municipality of Arteaga. Wilson et al. (2013a) estimated its EVS as 15, placing it in the lower portion of the high vulnerability
category. Its conservation status has been gauged as Least Concern by IUCN, but it is not listed by SEMARNAT. Photo by Michael
S. Price.
Amphib. Reptile Conserv. 61 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
No. 11. Sceloporus olivaceus Smith, 1934. The Texas Spiny Lizard is found from “northern central Texas southward through
the Gulf of Mexico coastal plain to southern Tamaulipas, westward nearly to the Big Bend area of Texas and eastern Coahuila”
(Lemos-Espinal et al. 2015: 239). This individual was encountered at Cafion el Chorro, in the municipality of Arteaga. Wilson et al.
(2013a) calculated its EVS as 13, placing it at the upper limit of the medium vulnerability category. Its conservation status has been
considered as Least Concern by IUCN; this species is not listed by SEMARNAT. Photo by Michael S. Price.
b a ie ys was e wa \e her a : A) ae Bt be > ‘
No. 12. Sceloporus ornatus Baird, 1859. The Ornate Spiny Lizard is a Mexican endemic species distributed in “southern and central
Coahuila” (Lemos-Espinal and Smith 2007: 303). This individual was found at ca. 8 km SW from Ejido Mayran, in the municipality
of San Pedro. Wilson et al. (2013a) determined its EVS as 16, placing it in the middle portion of the high vulnerability category.
Its conservation status has been calculated as Near Threatened by IUCN and as threatened (A) by SEMARNAT. Photo by Marco
Antonio Bazdn-Tellez.
Amphib. Reptile Conserv. 62 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
involved members of the Mennonite community in
Coahuila who were implicated in the clearing of 2,300
hectares of forest vegetation without authorization in the
municipality of Sierra Mojada; however, they managed
to escape legal sanction (https://www.eluniversal.com.
mx/estados/menonitas-de-coahuila-ganan-amparos-la-
profepa-por-2-mil-hectareas-de-predios).
Effect of roads. The state of Coahuila has an extensive
network of roads and highways, with a total of seven
federal highways. The total length of the road network
in the state is 8,336 km (Servicio Geolégico Mexicano
2017). During the period from 1980 to 2015, the
number of motor vehicles traveling within Coahuila
went from 149,242 to 741,515, an increase of 592,273
(or almost 400%!) in 35 years. The effect of roads on
the herpetofauna of the state remains to be studied, but
we assume that major highways might disrupt general
dispersion patterns and seasonal migration of some local
populations, and vehicles on municipal roads probably
simply run over many animals in large numbers.
Mining and energy projects. The history of Coahuila
is closely related to mining. It began as a leading
commercial activity in the colonial era, with the founding
of the city of Monclova and Minas de la Trinidad in 1577,
and later continued with the discovery and exploitation of
coal starting in 1828; copper in the Panuco mine in 1870;
zinc oxide, silver, and lead in Sierra Moyjada in 1879; and
silver, lead, and zinc in Reforma-Santa Teresa in 1890.
Most recently, the discovery and exploitation of fluorite,
celestite, sodium-magnesium salts, gypsum, barite, and
dolomite has been undertaken. Coahuila has an extensive
mining-metallurgical infrastructure, highlighted by the
metal foundry in Torreon, the iron foundry in Monclova,
coal plants in Nava, and several related processing plants
in various locations. The state of Coahuila contributed
3.1% of the value of national mining production in 2015,
occupying the first place in the production of iron, coal,
celestite, magnesium sulfate, sodium sulfate, bismuth,
and cadmium, second place in fluorite and silica, third
in barite and dolomite, fifth in stone aggregates, and in
smaller proportions plaster, sulfur, clays, gravel, sand,
limestone, gold, and silver. In addition, a large number
of unexplored geological areas have been reported in
Coahuila (Servicio Geolégico Mexicano 2017), for
example, the Hercules mine in the northwestern portion
of the state (http://www.thediggings.com/mines/2 1966;
accessed 20 July 2019), and those places are expected to
be sites for future development.
Natural gas production in the Burgos Basin. The
Burgos Basin is a shale deposit located in the northeastern
portion of Coahuila, directly south of the Rio Grande. It
is considered a great prospect for natural gas production
and covers a total area of 62,677 km’. The infrastructure
required to develop the production of natural gas is
Amphib. Reptile Conserv.
scheduled to be built in a timely manner during successive
10-year periods, and involves extensive extraction,
processing, and distribution facilities. It is expected that
the previous and on-going infrastructure projects will
have negative effects on the integrity of the habitat that
is used by the members of the regional herpetofauna
(http://energiaadebate.com/gas-de-lutitas-en-la-cuenca-
de-burgos/).
Wind turbines. In 2016, a wind farm consisting of 95
wind turbines was being built near Ejido Hipolito in the
Municipality of Ramos Arizpe, and another with 100
wind towers near Acufia, as well as a Solar Energy Park
in the Municipality of Viesca, which will be the largest in
Latin America and is planned to include more than two
million solar panels (http://coahuila.gob.mx/noticias/
index/avanza-parque-eolico-de-hipolito-24-07-16). The
Ramos Arizpe project covers an area of 4,754 hectares.
This requires, among other actions, the construction of
more than 50 km of access roads, an aerial transmission
line almost five km long, and an electrical substation
(http://proyectoeolicadecoahuila.com).
Elimination of herpetofauna due to cultural beliefs
and practices. Traditional beliefs and practices that
affect the herpetofauna of Coahuila are the same as
those previously reported for Nuevo Leon (Nevarez-de
los Reyes et al. 2016), likely due to their geographic
proximity and similar cultural backgrounds. Examples
include snakes being slaughtered due to fear and
superstition, misconceptions that many non-venomous
herpetofaunal species are venomous, and rattlesnakes
being consumed either for food or the belief that their
meat will prevent or cure cancer. It is obvious that
education is the key for reducing the needless killing of
these ecologically important denizens of Coahuila.
Use of pesticides. Agricultural activities in the state of
Coahuila are most intense in the arid region known as
Comarca Lagunera, where they are only possible due
to heavy irrigation using water from the Rio Nazas.
Although there is little information regarding this
problem, pesticides are commonly applied on Cantaloupe
(Cucumis melo) fields, one of the most important fruits
cultivated in the region (Vargas-Gonzalez et al. 2016).
That study found that in the agricultural cycle of 2010,
50 different active ingredients were used in the region;
26% of which were not authorized for use on cantaloupes
by COFEPRIS, and 46% of which were considered as
highly toxic to human health and the environment.
For example, six of them (carbofuran, endosulfan,
clorotalonil, mancozeb, imidacloprid, and metamidofos)
are regarded as among the most toxic to humans and the
environment.
Collecting and commercial trade. Currently, the
herpetofauna of Coahuila faces problems with unlawful
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
collecting and commercial trade that are similar to those
reported in Tamaulipas and Nuevo Leon (Teran-Juarez et
al. 2016; Nevarez-de los Reyes et al. 2016). Unfortunately,
these illegal activities have increased during the last few
years through social media. For example, based on our
personal observations, when photographs of rare species
are posted, it is common for collectors to be immediately
contacted by animal traffickers or pet owners ready to
purchase their specimens, or asked for specific localities.
Unfortunately, monitoring these activities remains
difficult, as does determining their true impact on the
local herpetofauna.
Fires involving natural habitats. Fires create a serious
threat to natural habitats in Coahuila, especially those
involving forested ecosystems. In 2017, 153 fires were
documented in the state beginning on 2 January and
ending on 23 December; thus, on average, a reported fire
occurred somewhere in the state every 2.4 days. Of the
38 municipalities in Coahuila, fires were recorded in 22
(57.9%) of them. The municipalities most often involved
were Arteaga (37 fires), Cuatro Ciénegas (12), Muzquiz
(11), Ramos Arizpe (23), and Saltillo (24). Three of these
municipalities (Arteaga, Ramos Arizpe, and Saltillo) are
located in the extreme southeastern portion of the state
where the state capital is located and where a majority of
the fires have occurred (84 of 153 fires, or 54.9%). The
number of ha involved in each of these 153 fires ranged
from 0.02 to 3,132. The largest of these fires took place
in the Municipality of San Buenaventura, at a locality
called, interestingly enough, El Quemado (“burned
by fire’). The total area burned in 2017 amounted to
10,289.6 ha, which is approximately 0.07% the total area
of Coahuila (15,159,500 ha).
At the time of this writing, information is also available
for the first 4.5 months of 2018 (10 January to 13 May)
(CONAFOR, Comisién Nacional Forestal Aspectos de
Incendios Forestales, —https://www.gob.mx/conafor).
During this period of time, 46 fires were reported, or one
fire in Coahuila every 2.9 days. Fires were registered
in 14 of the 38 municipalities in the state (36.8%).
These fires occurred most often in the Municipalities
of Muzquiz (15 fires), Cuatro Ciénegas (four), Arteaga
(three), Nadadores (three), Ocampo (three), and Saltillo
(three). Four of these six municipalities (Muzquiz,
Cuatro Ciénegas, Arteaga, and Saltillo) represent areas
with high fire occurrences during 2017 (see above). The
number of hectares burned in each fire during this 2018
period varied from 0.5 to 1,500. The largest fire took
place in Eutimias, in the Municipality of Ocampo, due to
lightning strikes. In general, the principal causes of these
fires, when known, were human negligence and lightning.
During this period, the total area burned was 4,198.3 ha
(about 0.03% of the state, or 31.3 ha/ day). This figure
compares to 28.2 ha/day in 2017. It appears likely that
the total number of hectares burned in Coahuila in 2018
should compare to those burned in 2017 (see above). The
Amphib. Reptile Conserv.
threat posed by fires will almost assuredly increase into
the future, given the human population growth in the
state of 7.5% from 2010 to 2015, which is higher than
the rate in Mexico as a whole (6.8%; http://wikipedia.
org; accessed 5 July 2018).
Lazcano et al. (2006) reported finding a Wiegmann’s
Alligator Lizard (Gerrhonotus liocephalus) killed by a
forest fire in the neighboring state of Nuevo Leon and
advised that only additional investigations would be
able to determine the demographic consequences of this
sort of mortality. Banda-Leal et al. (2018) documented
for the first time the distribution of Gerrhonotus parvus
in Coahuila, and mentioned finding some specimens of
this species in the Sierra Zapalinamé that had died from
forest fires.
Conservation Status
The discussion of the conservation status of members
of the Coahuilan herpetofauna follows the same three
systems of conservation assessment as used in the other
entries 1n the Mexican Conservation Series. These
systems are those found in SEMARNAT (2010), the
IUCN Red List (http://tucnredlist.org), and the EVS
(Wilson et al. 2013a,b). The assessments from these three
systems were updated as needed.
The SEMARNAT System. SEMARNAT (Secretaria
del Medio Ambiente y Recursos Naturales) is the
environmental ministry of Mexico, and it is “charged with
the mission of protecting, restoring, and conserving the
ecosystems, natural resources, assets and environmental
services of Mexico with the goal of fostering sustainable
development’ (http://www.semarnat.gob.mx/conocenos/
quienessomos; accessed 7 January 2019). In 2010, this
agency published the Norma Oficial Mexicana (Official
Mexican Standard)-059, which deals with the protection
of the native members of the Mexican flora and fauna and
establishes categories of risk. This system is commonly
used by Mexican herpetologists to discuss various
segments of the country’s herpetofauna. Its utility for work
on the herpetofauna of Coahuila has also been assessed.
The SEMARNAT system comprises three categories,
including Endangered (P), Threatened (A), and Special
Protection (Pr). For a Mexican species not evaluated
using one of these three categories, it is designated here
as having no status (NS). The SEMARNAT evaluations
are shown in Table 7 and summarized in Table 9.
Unfortunately, the SEMARNAT assessments are
not very useful here, as most species in Coahuila remain
unevaluated (90 of 140 native species; 64.3%). Thus,
evaluations of conservation status are available for only
50 species (35.7%). Of these 50 species, 23 (46.0% of
the total) are judged as species of Special Protection (Pr):
Anaxyrus debilis, Gastrophryne olivacea, Lithobates
berlandieri, Ambystoma velasci*, Aquiloeurycea
scandens*, Chiropterotriton priscus*, Gerrhonotus
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
—— ‘a og = a pen . +e — ae < : :
ee ee “ id ee oe -.
vicinity of Estacién Marte, in the municipality of General
Cepeda. Photo by Manuel Nevarez de los Reyes.
Fig. 19. Impact of Roads. Masticophis flagellum dead on the
road near El Mimbre, in the municipality of Parras. Photo by
Manuel Nevarez de los Reyes.
Fig. 21. Mining Projects. Mining of materials for construction
near Paso de Carneros, in the municipality of Saltillo. Photo by
Manuel Nevarez de los Reyes.
parvus, Gambelia wislizenii, Coleonyx brevis, Coleonyx
reticulatus, Sceloporus grammicus, S. maculosus*,
Scincella lateralis, Crotalus atrox, C. lepidus,C. molossus,
C. pricei, C. scutulatus, C. viridis, Sistrurus tergeminus,
Terrapene ornata, Kinosternon hirtipes, and Apalone
spinifera. These 23 species include four that are endemic
to Mexico (indicated by asterisks); and all of the 19 non-
endemic species are shared with the United States. The
Amphib. Reptile Conserv.
= =
Fig. 18. Deforestation for Ranching Purposes. Cattle in the mu-
nicipality of Francisco I. Madero. Photo by Manuel Nevarez de
los Reyes.
Fig. 20. Mining Projects. Mineral charcoal mining exploitation,
in the municipality of Nava. Photo by Manuel Nevarez de los
Reyes.
Fig. 22. Energy Projects. Wind generation of electricity near
Hipolito, in the municipality of Ramos Arizpe. Photo by Manu-
el Nevarez de los Reyes.
remaining 27 species are assessed as either Endangered
(P) or Threatened (A). The Endangered species
amount to four: Uma exsul, U. paraphygas, Gopherus
flavomarginatus, and Apalone atra (Table 7); three are
endemic to Coahuila and one is endemic to Mexico.
Twenty-three species are considered as Threatened:
Aquiloeurycea galeanae, Crotaphytus collaris, C.
reticulatus, Cophosaurus texanus, Holbrookia lacerata,
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The herpetofauna of Coahuila, Mexico
Table 9. SEMARNAT categorizations for herpetofaunal species in Coahuila, Mexico, arranged by families. Non-native species are
not included.
Number SEMARNAT Categorizations
Families of
. Special No status
species Endangered (P) | Threatened (A) protection (Pr) (NS)
(ee eee
Craugastoridae eee
Eleutherodactylidae a | Sy
Hylidae ee ee
Microhylidae ee
Ranidae Ee
Scaphiopodidae a. ac | a — as
Subtotals es
Ambystomatidae SSS Se
Plethodontidae SS a |
Subtotals ESS Sees
Totals Se ee eee
Anguidae _—EE ET Se
Crotaphytidae | Ss ee
Eublepharidae ——S SS
Phrynosomatidae
Scincidae (Se SS
Sphenomorphidae EE a ae
Teiidae ES ae
Xantusiidae a a
Subtotals a a kas)
Colubridae EE EEE
Dipsadidae a Ss |e ee
Elapidae aS a
Leptotyphlopidae ee ee
Natricidae SS ae
Viperidae ee
Subtotals ee (es
Emydidae ES ae
Kinosternidae =
Testudinidae
—)
a ha
a a ae
l
7
1
3
1
a
PS)
Phrynosoma_ orbiculare, Sceloporus ornatus, Uta The IUCN System. The system of conservation
stansburiana, Scincella silvicola, Coluber constrictor, categorization developed by the International Union for
Lampropeltis alterna, Masticophis flagellum, Pituophis — the Conservation of Nature (IUCN) is applied globally,
deppei, Tantilla atriceps, T. gracilis, Trimorphodon _ theoretically to all organisms, and consists of a set of
vilkinsonii, Nerodia erythrogaster, Thamnophis exsul, T; nine categories, divided into four general categories,
marcianus, T: proximus, Pseudemys gorzugi, Terrapene including: Extinct (Extinct and Extinct in the Wild),
coahuila, and Gopherus berlandieri. This group of 23. Threatened (Critically Endangered, Endangered, and
species includes a curious mixture of seven country and ~—- Vulnerable), Lower Risk (Near Threatened and Least
state endemic species and 16 relatively broadly ranging Concern), and other categories (Data Deficient and Not
non-endemic species, some with extensive ranges inthe — Evaluated). Those evaluations applying to the Coahuilan
United States. herpetofauna are shown in Table 7 and summarized in
Until such time as SEMARNAT provides conservation — Table 10.
evaluations for all Mexican herpetofaunal species, this Only 14 of 140 native species (10.0%) are judged to
system will continue to have only limited utility for | be Threatened. No species are considered to be Critically
conservation purposes. Endangered; seven are assessed as Endangered; and seven
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Lazcano et al.
Table 10. IUCN Red List categorizations for herpetofaunal families in Coahuila, Mexico. Non-native species are excluded. The shaded
columns to the left are the “threat categories,” and those to the right are the categories for which either too little information on conservation
status exists to allow the taxa to be placed in any IUCN category, or they have not been evaluated.
Families
| Subtotals | 19
| Ambystomatidae |
| Plethodontidae | 3
Number IUCN Red List categorizations
of
23
5
4
2
29
C)
3
4
29
4
]
3
7
10
54
5
3
2
2
12
117
140
51
others as Vulnerable. The seven Endangered species
are: Gerrhonotus parvus*, Crotaphytus antiquus*”,
Sceloporus cyanostictus*, S. goldmani*, Uma exsul**,
Terrapene coahuila**, and Trachemys taylori**. Three
of these species are country endemics and four are state
endemics. The seven Vulnerable species (VU) are:
Eleutherodactylus longipes*, Aquiloeurycea scandens*,
Crotaphytus reticulatus, Sceloporus maculosus*, Storeria
hidalgoensis*, Trachemys gaigeae, and Gopherus
flavomarginatus*. Five of the seven VU species are
country endemics; the remainder are non-endemics. The
Lower Risk species amount to 102 species, constituting
72.9% of the native species in the state (Table 10). Of
these 102 species, eight are Near Threatened and 94
Amphib. Reptile Conserv.
67
are Least Concern. As has been demonstrated clearly in
other studies in the Mexican Conservation Series, the
allocation of such a large number of species to the Least
Concern category seems unjustified and the conservation
status of these 94 “Least Concern” species is examined in
greater detail in the following section.
Only a single Coahuilan species is considered to be
Data Deficient (Table 10): Kinosternon durangoense
(Table 7). This turtle is a country endemic that was
recognized as a distinct species in 2001 (Serb et al. 2001)
by being elevated from a subspecies of K. flavescens, but
very little information on its biology and conservation
status 1s available to date. Therefore, this appears to be a
sound assessment.
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
No. 13. Sceloporus samcolemani Smith and Hall, 1974. Coleman’s Bunch Grass Lizard is a Mexican endemic species that ranges
from “extreme southeastern Coahuila and southern central Nuevo Leon” (Watkins-Colwell et al. 1998: 675.2). This individual
was seen at Monterreal, in the municipality of Arteaga. Wilson et al. (2013a) gauged its EVS as 15, placing it in the lower portion
of the high vulnerability category. Its conservation status has been determined as Least Concern, but this lizard is not listed by
SEMARNAT. Photo by Michael S. Price.
No. 14. Uma exsul Schmidt and Bogert (1947). The Fringe-toed Sand Lizard is a Mexican endemic species occurring in extreme
southwestern and south-central Coahuila (Lemos-Espinal and Smith 2007). This individual was located at ca. 2 km SW from Ejido
Alejandria, in the municipality of San Pedro. Wilson et al. (2013a) assessed its EVS as 16, placing it in the middle portion of the
high vulnerability category. Its conservation status is evaluated as Endangered by IUCN and as endangered (P) by SEMARNAT.
Photo by Marco Antonio Bazdn-Tellez.
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Lazcano et al.
No. 15. Plestiodon dicei (Ruthven my Ge 1933). Bick: S Rho noel Skink j is a ars Meanie occurring from central
Nuevo Leon eastward to central and southern Tamaulipas (Feria-Ortiz et al. 2011). This individual was found in Monterreal, in the
municipality of Arteaga. Wilson et al. (2013a) calculated its EVS as 12, placing it in the upper portion of the medium vulnerability
category. Its conservation status has not been evaluated by IUCN and this species is not listed by SEMARNAT. Photo by Eli Garcia
Padilla.
No. 16. Bogertophis subocularis (Brown, 1901). The Trans-Pecos Rat Snake is distributed “in southern New Mexico, southwestern
Texas, and in northeastern Mexico, from Chihuahua through Coahuila and into Nuevo Leon and through Durango down to its border
with Zacatecas” (Lemos-Espinal et al. 2015: 318). This individual came from Cuatrociénegas, in the municipality of Cuatrociénegas
de Carranza. Wilson et al. (2013a) judged its EVS as 14, placing it at the lower edge of the high vulnerability category. Its conservation
status is evaluated as Least Concern by IUCN, but it is not listed by SEMARNAT. Photo by Michael S. Price.
Amphib. Reptile Conserv. 69 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Twenty-three species (16.4%) in the native Coahuilan
herpetofauna remain unevaluated (Table 10). The status
of these species is examined further using the EVS
system in the following section.
The EVS System. The EVS system, developed
originally for use in the conservation assessment of the
Honduran herpetofauna (Wilson and McCranie 2004),
has been applied subsequently to the entirety of Mexico
(Wilson et al. 2013a,b) and to Central America (Johnson
et al. 2015b), as well as to various states and groups
of states in Mexico (Alvarado-Diaz et al. 2013; Mata-
Silva et al. 2015; Johnson et al. 2015a; Teran-Juarez et
al. 2016; Woolrich-Pifia et al. 2016, 2017; Nevarez-de
los Reyes et al. 2016; Cruz-Saenz et al. 2017; Gonzalez-
Sanchez et al. 2017). Wilson et al. (2013a,b) described
the use of this system for the herpetofauna of Mexico;
and it is employed here to assess the conservation status
of the herpetofauna of Coahuila (see data in Table 7,
summarized in Table 11).
The total range of EVS values for the herpetofauna of
Coahuila spans the entire theoretical EVS range (3—20).
The most frequent values (more than 10 species) are nine
(10), 10 (10), 11 (12), 12 (17), 13 (17), 14 (14), 15 (13),
and 16 (12). These eight scores were applied to a total
of 104 species, or 74.3% of the total number of native
species. The average EVS value is 12.1 (1,693/140). When
allocated to the three summary categories of low (3-9),
medium (10-13), and high (14—20), the species counts for
these categories are 32, 56, and 52, respectively.
The lowest EVS value of 3 was applied to three
species of anurans (Rhinella horribilis, Smilisca baudinii,
and Scaphiopus couchii), which are geographically and
ecologically widespread and have the most widespread
reproductive mode (eggs and tadpoles in still water).
At the other extreme, one species (the trionychid turtle
Apalone atra) was provided a value of 20, because of
its narrow geographic and ecological distribution and its
high level of human persecution.
Comparing the results of the IUCN categorization
with those of the EVS system in Table 12, indicates that
14 of the 52 high vulnerability species (26.9%) are judged
to occupy one of two IUCN threat categories (EN or VU,
note that no species are allocated to the CR category).
Seven species (five lizards and two turtles) are evaluated
as EN, and seven as VU (one anuran, one salamander,
two lizards, one snake, and two turtles). These 14
species comprise 10.0% of the 140 native herpetofaunal
species in Coahuila. At the opposite extreme, the 32
low vulnerability species comprise 35.1% of the 93
LC species. As in other Mexican Conservation Series
studies, the results of the applications of the IUCN and
EVS systems do not complement one another.
Twenty-four species remain unassessed using the
IUCN system (allocated to the NE category in Table 7).
Four of these species are state endemics (Gerrhonotus
mcecoyi, Sceloporus gadsdeni, Scincella_ kikaapoa,
Amphib. Reptile Conserv.
and Apalone atra), five are country endemics (Barisia
imbricata, Holbrookia approximans, Plestiodon dicei,
Lampropeltis leonis, and Crotalus morulus), and the
remainder are non-endemics. The range of EVS values
for these 24 species is 6-20, which places some of them
into each of the three summary categories (Table 13).
Four have low EVS scores, ten have medium scores,
and ten have high scores. Until such time as IUCN
evaluations are available for these species, we suggest
that the high EVS species should be placed in one of
the three threat categories, perhaps as follows: CR—
Gerrhonotus mccoyi, Sceloporus gadsdeni, Scincella
kikaapoa, Lampropeltis leonis, Crotalus morulus,
Apalone atra; EN—Barisia imbricata, Holbrookia
approximans, VU—Aspidoscelis marmorata, Salvadora
deserticola. We also suggest that the species with EVS of
12 or 13 be placed in the NT category. The remainder of
the species with EVS of 6-11 can be allocated to the LC
category (Table 13).
As with other studies in the Mexican Conservation
Series, this study found that a significantly large number
of the Coahuilan herpetofauna members have been
allocated by the IUCN to the Least Concern category.
The number of such species amounts to 93 (66.4% of the
total of 140 species). Given that almost seven of every
ten herpetofaunal species in Coahuila is judged Least
Concern, it might appear that the state herpetofauna is in
relatively good shape with respect to conservation status.
In order to ascertain whether such an optimistic view is
the case, the 93 species in Table 14 were placed along
with the calculations for their respective EVS values.
Although one might expect that the LC species would
most likely be non-endemic to Mexico, this analysis
found that 12 are country endemics, including one
salamander, nine lizards, and two snakes, and one lizard
is a state endemic (Table 14). The range of EVS values
for these 93 species is 3—18, or only slightly less than the
entire theoretical range for EVS (3-20). The allocation of
the EVS values for the 93 species into the three summary
categories demonstrates the following: low (3—9)—27;
medium (10-13)—45; and high (14—-20)—22. Based
on these allocations, we suggest that a more realistic
assessment would place the 22 high vulnerability
species in one of the three IUCN threat categories, as
follows: CR (Gerrhonotus lugoi, Thamnophis exsul,
and Gopherus berlandieri),; EN (Coleonyx reticulatus,
Sceloporus cautus, S. couchii, S. parvus, S. samcolemani,
Xantusia extorris, Lampropeltis mexicana, Pantherophis
bairdi, and Apalone spinifera); and VU (Coleonyx brevis,
Cophosaurus texanus, Sceloporus minor, Aspidoscelis
inornata, A. tesselata, Bogertophis subocularis,
Lampropeltis alterna, Pituophis deppei, Agkistrodon
laticinctus, and Crotalus pricei). We also suggest that
the 43 medium vulnerability species probably should
be placed in the NT category, and that the 27 low
vulnerability species could remain in the LC category.
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
PEE EEDELE DEEL EELLTERED EDEL EL [Ee
PAPEETE EEDA EEDE EERE EDEL
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Number
of
Species
Families
Leptotyphlopidae
Category Totals
Natricidae
Sphenomorphidae
Viperidae
Ambystomatidae
Plethodontidae
Subtotals
Kinosternidae
Testudinidae
Trionychidae
Subtotals
Totals
Sum Totals
Scincidae
Xantustidae
Subtotals
Colubridae
Dipsadidae
Elapidae
Subtotals
Emydidae
Table 11. Environmental Vulnerability Scores (EVS) for herpetofaunal species in Coahuila, Mexico, arranged by family. Shaded area to the left encompasses low vulnerability scores, and the
Subtotals
one to the right high vulnerability scores. Non-native species are excluded.
Amphib. Reptile Conserv. 71 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 12. Comparison of Environmental Vulnerability Scores (EVS) and applicable IUCN categorizations for members of the
herpetofauna of Coahuila, Mexico. Non-native species are excluded. No species are allocated to the CR IUCN categories. Shaded
area at the top encompasses low vulnerability category scores, and the one at the bottom high vulnerability category scores.
IUCN Categories
Mi Near
Vulnerable ‘Tivventétied
Endangered
3
4
7
—
—
S
10
]
3
]
2
7
Table 13. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Coahuila, Mexico, currently not evaluated
(NE) by the IUCN. Non-native taxa are not included. * = country endemic species; ** = state endemic species.
Environmental Vulnerability Score
Geographic Ecological Heprouucliye
Ps OE ST Ae Mode/Degree of Total Score
Distribution Distribution ‘
Persecution
12
Acris blanchardi
Barisia ciliaris*
Gerrhonotus mccoyi**
Holbrookia approximans*
Sceloporus cowlesi
Sceloporus cyanogenys
Sceloporus gadsdeni**
Sceloporus marmoratus
Plestiodon dicei*
Scincella kikaapoa**
Aspidoscelis marmorata
Lampropeltis annulata
Lampropeltis gentilis
Lampropeltis leonis*
Lampropeltis splendida
Salvadora deserticola
Sonora episcopa
Heterodon kennerlyi
Hypsiglena jani
Leptodeira septentrionalis
Rena segrega
Crotalus morulus
Crotalus ornatus
Apalone atra**
Amphib. Reptile Conserv. 42 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 14. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Coahuila, Mexico, assigned to the IUCN
Least Concern category. Non-native taxa are not included. * = country endemic species; ** = state endemic species.
Environmental Vulnerability Score
: : Reproductive
T:
ae Geographic Eeoloeicg! Mode/Degree of Total Score
Distribution Distribution :
Persecution
5 5
Anaxyrus cognatus 1
Anaxyrus debilis
Anaxyrus punctatus
—
N
Anaxyrus Speciosus
—
Oo
Anaxyrus woodhousii
Incilius nebulifer
Rhinella horribilis
Craugastor augusti
—
N
Eleutherodactylus cystignathoides
—
—
Eleutherodactylus guttilatus
Dryophytes arenicolor
Smilisca baudinii
Gastrophryne olivacea
Lithobates berlandieri
Scaphiopus couchii
Spea multiplicata
—
is)
Ambystoma velasci*
—
ies)
Gerrhonotus infernalis
—
Oo
Gerrhonotus lugoi**
—
ies)
Crotaphytus collaris
—
bo
Crotaphytus wislizenii
—
~
Coleonyx brevis
—
N
Coleonyx reticulatus
—
™~
Cophosaurus texanus
Phrynosoma cornutum
Phrynosoma modestum
—
N
Phrynosoma orbiculare*
—
N
Sceloporus cautus*
—
Nn
Sceloporus couchii*
Sceloporus grammicus
Sceloporus magister
—
Oo
Sceloporus merriami
—_
—
Sceloporus minor*
—
ies)
Sceloporus olivaceus
—
N
Sceloporus parvus*
—
N
Sceloporus poinsettii
—
N
Sceloporus samcolemani*
—
N
Sceloporus spinosus*
—
oO
Urosaurus ornatus
Uta stansburiana
Plestiodon obsoletus
—
N
Plestiodon tetragrammus
—
ies)
Scincella lateralis
—
N
Scincella silvicola*
Aspidoscelis gularis
—
i
Aspidoscelis inornata
—
™~
Aspidoscelis tesselata
—
N
Xantusia extorris*
Arizona elegans
—
Bogertophis subocularis
—
os)
Coluber constrictor
TEER THETEPRRER HHT {tHE
HHA RTH TRE
TREE
TEPEEPPTTCPPEEE RTP {TTP
Amphib. Reptile Conserv. 73 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 14 (continued). Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Coahuila, Mexico, assigned
to the IUCN Least Concern category. Non-native taxa are not included. * = country endemic species; ** = state endemic species.
Geographic
Distribution
4
Diadophis punctatus
Nerodia erythrogaster
Tantilla nigriceps
Tantilla wilcoxi
Nerodia rhombifer
Trimorphodon vilkinsonii
Apalone spinifera
Relative Herpetofaunal Priority
Johnson et al. (2015a) developed the concept of Relative
Herpetofaunal Priority (RHP), a simple means for
measuring the relative importance of the herpetofaunal
species found in any geographic entity (e.g., a state or
a physiographic region). Determining the RHP involves
the use of two methods, i.e., (1) calculating the proportion
Amphib. Reptile Conserv.
Environmental Vulnerability Score
Reproductive
Mode/Degree of
Persecution
Ecological
Distribution
Total Score
of state and country endemics relative to the entire
physiographic regional herpetofauna, and (2) computing
the absolute number of EVS high category species in
each physiographic regional herpetofauna.
Here, two tables have been constructed to ascertain
the RHP values for the Coahuilan herpetofauna, one for
the endemicity values (Table 15) and the other for the
high category EVS values (Table 16). The data in Table
74 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 15. Numbers of herpetofaunal species in four distributional categories among the 10 physiographic provinces of Coahuila,
Mexico. Rank determined by adding state and country endemics.
Physiographic Province Non- Country State Non-
ae endemics endemics endemics natives
5 2 2
Llanuras de Coahuila y Nuevo Leon
36
42
35
43
37
4]
32
32
50
Cs
]
ir ee
= a a a a
rhe ee eS ae
15 demonstrate that the highest amount of endemicity is
found in the Gran Sierra Plegada, only a small portion
of which is located in Coahuila (Fig. 1); thus, this region
occupies rank number 1 using this measure. Of the 51
species recorded in this region, 18 are country endemics
(35.3%). Nevarez-de los Reyes et al. (2016) found a
similar situation prevailing in the neighboring state
of Nuevo Leon, in which 33 of 87 species (37.9%) in
this same region consist of country and state endemics.
Rank number 2 is occupied by the Sierras Transversales
located along the southern border of Coahuila, in which
13 of 46 species (28.3%) are country endemics. The
remaining eight physiographic regions occupy ranks 3
through 7, given that several of these regions share the
same rank with other regions (Table 15). One region
(Sierras y Llanuras Coahuilenses) occupies rank 3, and
contains eight country and state endemics. Only one
region occupies rank 4, which is the Bolson de Mapimi,
with five country endemics and two state endemics. One
region (Pliegues Saltillo Parras) lies at rank 5, with six
country endemics. Two regions (Laguna de Mayran and
Sierra de la Paila) occupy rank 6, with two endemics
each. Finally, there are three regions (Llanuras y Sierras
Volcanicas, Serranias del Burro, and Llanuras de
Coahuila y Nuevo Leon) that occupy rank 7, each with a
single endemic species.
The numbers of species for each of the 10
physiographic regions are placed into the three EVS
—tRee
CO | LW
categories (low, medium, and high) in Table 16.
These data indicate that the greatest number of high
vulnerability species (22 of 88, 25.0%) is found in the
Sierras y Llanuras Coahuilenses in the central portion of
the state (Fig. 1), thus this region occupies rank number
1. The next highest number (17 of 50 species, or 34.0%)
is found in the Gran Sierra Plegada, which is located in
the southeastern corner of the state (Fig. 1) and occupies
rank number 2. The 3 rank is occupied by the Sierras
Transversales, with 14 high-vulnerability species out
of 46 (30.4%). The numbers of high EVS species in the
remaining seven regions range from seven to 13.
The rankings obtained by using these two RHP
methods are not identical, but at least the regions
occupying ranks | through 3 are the same three regions 1n
each case, as follows (endemic species ranking followed
by high vulnerability ranking):
Gran Sierra Plegada (1, 2)
Sierras Transversales (2, 3)
Sierras y Llanuras Coahuilenses (3, 1)
The results of this RHP analysis clearly show that
the most important region in the state is the Gran Sierra
Plegada, occupying rank 1 for endemic species and
rank 2 for high vulnerability species. This finding is
interesting, given the small amount of this physiographic
region situated in Coahuila (2,178 km”, as noted above),
Table 16. Number of herpetofaunal species in the three EVS categories among the 10 physiographic regions of Coahuila, Mexico.
Rank determined by the relative number of high EVS species. Non-native species are excluded.
Rank
Order
Amphib. Reptile Conserv.
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
a . ’ Cs . = 7 ees lee” a
r ee ee . a eh ome aii ae oe
~ tlP ra ~~
mt, xs ae any ad . } Ros < “ue ae ee ; 4 he
et Laces ee a . PD ee Sou ment
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No. 17. Rhinocheilus lecontei Baird and Girard, 1853. The Long-nosed Snake occurs from “California to Kansas, excluding much
of the Great Basin and the Rocky Mountains, southward to Baja California and Nayarit and, east of the Sierra Madre [Occidental],
to the southern limited of the Chihuahua Desert” (Lemos-Espinal et al. 2015: 371). This individual was located at ca. 4 km east of
Nava, in the municipality of Nava. Wilson et al. (2013a) assessed its EVS as 8, placing it in the upper portion of the low vulnerability
category. Its conservation status is judged as Least Concern by IUCN, but it is not listed by SEMARNAT. Photo by Marco Antonio
Bazdn-Tellez.
a ee aes Se = -«< .a 4 ™
No. 18. Zantilla atriceps (Gunther, 1895). The Mexican Black-headed Snake is distributed from “extreme southern Texas southward
through central Coahuila to extreme northeastern Durango and northern Tamaulipas and San Luis Potosi” (Lemos-Espinal et al.
2015: 382). This individual came from Rancho La Boca, on the border of the municipalities of Bustamante and Mina. Wilson et al.
(2013a) calculated its EVS as 11, placing it in the lower portion of the medium vulnerability category. Its conservation status has
been considered as Least Concern by IUCN, and as a threatened species (A) by SEMARNAT. Photo by Michael S. Price.
Amphib. Reptile Conserv. 76 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
o
No. 19. Micrurus tener (Baird and Girard, 1853). The Texas Coralsnake occurs “from the Mississippi River westward into Texas,
in the United States, and in Mexico, from Tamaulipas south to Veracruz...” (Lemos-Espinal and Dixon 2013: 240). This individual
came from ca. 16 km east of Nava, in the municipality of Nava. Wilson et al. (2013a) calculated its EVS as 11, placing it in the
middle of the medium vulnerability category. Its conservation status has been determined as Least Concern by IUCN, and this
species is not listed by SEMARNAT. Photo by Marco Antonio Bazan-Tellez.
(ied a
- Wide ie
es s
a -* .
~~ “< 8, — =
_ —- P
F ~~ 2S
+
- A,
. — na — - 2 —— = = =
-_— = : : =. + . ail ies
. -—
- ~~
No. 20. Crotalus atrox Baird and Girard, 1853. The Western Diamondback Rattlesnake occupies “much of the southwestern USA
south to northeastern Baja California, Sonora and northern Sinaloa, and east of the Sierra Madre Occidental from Chihuahua east to
Tamaulipas and south to Hidalgo and Veracruz” (Rorabaugh and Lemos-Espinal 2016: 573). This individual was found at ca. 1 km
NW from Ejido Mieleras, in the municipality of Viesca. Wilson et al. (2013a) determined its EVS as 9, placing it at the upper limit
of the low vulnerability category. Its conservation status is judged as Least Concern by IUCN and as a species of special protection
(Pr) by SEMARNAT. Photo by Marco Antonio Bazdn-Tellez.
Amphib. Reptile Conserv. 77 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
although it has considerably more area outside the
state. The two other regions indicated above (Sierras
Transversales and Sierras y Llanuras Coahuilenses) are
considerably larger. The Gran Sierra Plegada supports 18
country endemics (Table 15) and 17 high vulnerability
species (Table 16). The Sierras Transversales contains 13
country endemics (Table 15) and 14 high vulnerability
species (Table 16); the respective figures for the Sierras
y Llanuras Coahuilenses are eight endemic species and
22 high vulnerability species. The level of protection
provided for these various species is indicated in the
following section on protected areas.
Protected Areas in Coahuila
A system of formally protected areas is integral to any
effort to protect any portion of the planetary biota from
the principal anthropogenic impacts brought about by
habitat degradation and destruction. Ostensibly, such a
system should incorporate as much of the environmental
diversity that exists within the target region (in this
case, the state of Coahuila) and as large of a portion of
that patrimony as is feasible within existing economic
confines. In an effort to determine how these concerns
have been addressed in Coahuila, information on
the protected areas in the state has been collated and
presented in Table 17.
The data in Table 17 indicate that of the 19 protected
areas listed, eight are federal reserves, four are federal/
private reserves, three are state reserves, three are state/
private reserves, and one is a municipal reserve. The
eight areas administered at the federal level include one
biosphere reserve, one national park, three floral and
faunal protection areas, two resource protection areas,
and one national monument.
These 19 areas in Coahuila have been established over
the 100 years from 1915 to 2015. Thirteen of these 19
areas have been in existence only since the turn of the
century or thereafter, while three were established in the
decade of the 1990s, two in the decade of the 1940s, and
one in 1915. Thus, it remains to be seen in the analysis
of the remainder of the data in Table 17 exactly what has
been accomplished in these areas, especially since 68.4%
of them (13/19) have existed for fewer than 17 years.
The areas of coverage of these protected areas range
broadly from as low as 38 ha to as high as 1,519,385 ha.
Interestingly, the largest of the 19 areas is the Area de
Proteccion de Recursos Naturales Cuenca Alimentadora
del Distrito Nacional de Riego 04 Don Martin,
established in 1915, which 1s the one with the longest
existence. The total coverage of these areas is 2,717,443
ha or approximately 27,174 km?, which is 17.9% of the
area of Coahuila. Portions of these 19 areas are located in
23 of the 38 municipalities (60.5%).
This system of protected areas in the state contains
representatives of eight of the ten physiographic regions,
including the Bols6n de Mapimi (one of 20 areas),
Amphib. Reptile Conserv.
Llanuras y Sierras Volcanicas (two), Laguna de Mayran
(one), Sierras y Llanuras Coahuilenses (eight), Serranias
del Burro (two), Sierra Transversales (four), Gran Sierra
Plegada (four), and Llanuras de Coahuila y Nuevo
Leon (two). The two regions with no representation are
the Sierra de la Paila and the Pliegues Saltillo Parras.
It is no doubt fortuitous that the three physiographic
regions with the greatest amount of representation in
the protected areas system are the regions having the
great herpetofaunal significance, 1.e., the Gran Sierra
Plegada, Sierras Transversales, and Sierras y Llanuras
Coahuilenses. Unfortunately, however, of the protected
areas for which such information is available, all are
known to be occupied to some extent by landowners.
Management plans are known to be available for only
five of the federal protected areas, which points out the
great need for completion of such plans for the remainder
of the areas. Even less well represented are herpetofaunal
surveys, of which there are only three completed and
three in the process of completion. Completion of the
remainder of the surveys needs to be undertaken as soon
as possible.
In general, systems of protected areas are established
without consideration of the conservation needs of the
herpetofauna, so it 1s not surprising that this need is
still outstanding in Coahuila. The good news is that the
physiographic regions that are herpetofaunally most
important, based on our RHP analyses, are those best
supplied with protected areas. The bad news is that sizable
proportions of those areas are occupied by landowners,
have no management plans designed, and have been
subject to no herpetofaunal surveys. Thus, at present,
there is no chance of answering any of the more pressing
questions about the state of population sustainability
of the component species of Coahuila’s herpetofauna.
So, redressing these inadequacies in the design and
implementation of the protected areas system has to be
undertaken so that the ability of the current system of
protected areas to provide for perpetual protection of the
state’s herpetofauna can be assessed and strengthened.
Here, the expected herpetofaunal content of the 19
protected areas in Coahuila is catalogued by compiling
the species known to occupy the physiographic regions
represented in each of these regions. We employed this
means since too few herpetofaunal surveys have been
undertaken in these areas to date. Thus, ground-based
field surveys will be necessary to provide the empirical
data required to substantiate the actual herpetofaunal
content of the state’s protected areas. Using this approach,
the results are shown in Table 18, and summarized in
Table 19.
Of the 143 species recorded in Coahuila, 120 (83.9%)
are expected to be found in one or more of the 19 protected
areas (Table 19). The number of species expected to
occur in each area ranges from three in the Parque
Estatal Bosque Urbano Ejército Mexicano to 84 in the
Area de Proteccién de Flora y Fauna Cuatro Ciénegas.
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
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October 2019 | Volume 13 | Number 2 | e189
79
Amphib. Reptile Conserv.
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The herpetofauna of Coahuila
October 2019 | Volume 13 | Number 2 | e189
80
Amphib. Reptile Conserv.
Lazcano et al.
Table 18. Distribution of herpetofaunal species in Natural Protected Areas of Coahuila, Mexico, based on estimated inclusions. Abbreviations are as
follows: * = species endemic to Mexico; ** = species endemic to Coahuila; and *** = non-native species.
Natural Protected Area
Taxa ‘ : :
[Anora G@specie)
[Butonitae 7 specie
Angas cognats
[Amcgras debs
Angra puncahs
[Ancyras spcios
[énciyas woodkous
nce neler
Rhinela horrible
[Crangastoridae (Usps)
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[craugasor angus
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Eleutherodactylus cysthignathoides
Eleuthera
A a
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sed Ei] Ess] al pte ie [et] | Tala
i | I [ee ea ae
eal Ee el Ee ee Ee
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Hylidae (1 species)
Dryophytes arenicolor
[Gastophene otvacea
PRankse @ pects)
ithobaesberlandieh ——
Lithobes testes
Seaphiopodine @ pecs)
Seaphioms cowh
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Squamate @3 sped)
TAnguite species)
+
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Gerrononusparns®
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[crotaniyasaniguas**
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fe Sa AS SS |
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Da tS a a a 50) S| |
JL ca i | a a |
Amphib. Reptile Conserv. 81 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 18 (continued). Distribution of herpetofaunal species in Natural Protected Areas of Coahuila, Mexico, based on estimated inclusions.
Abbreviations are as follows: * = species endemic to Mexico; ** = species endemic to Coahuila; and *** = non-native species.
ee Bes See
Sierra de Zapalinamé
Sierra San Vicente
Cafion del Diablo
Rancho La Puerta
October 2019 | Volume 13 | Number 2 | e189
Rancho Media Luna
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Lazcano et al.
Table 18 (continued). Distribution of herpetofaunal species in Natural Protected Areas of Coahuila, Mexico, based on estimated inclusions.
Abbreviations are as follows: *
= non-native species.
‘and ***
>
= species endemic to Coahuila
Natural Protected Area
oR OK
>
= species endemic to Mexico;
PI Tall! BER Meese eee eee see
ee
men) | OY I Ys IES Ee JE fe a SI a Lif if
pinnae carne PEI | IRIE Sey ae a ea eet
piseeeeiceien NU) a) a I | | ees | If
See dd Pe
epost ITA) LYRE fi | SIRE Yah |) |S 1a
moisten IT | AUPE ERIE Ih if | ai al el SA RE Pa]
pyoRiosntown | | [+l+] | | | | TT | Tt tt deded+t Tt eT TEE
a a A i IS ee i
Los Novis a Ra a Ce | |
Meindl |e ee EE EEE ee
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come Ze eee Re ee Ren eaee eee
ponder _1]5 [0] | |S a | Se ee |e eS]!
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ela a a] EE
ona elegans
Colubridae (26 species)
Ariz
Coluber constrictor
Gyalopion canum
Lampropeltis leonis*
Lampropeltis splendida
Masticophis flagellum
Opheodrys aestivus
Tantilla atriceps
Tantilla gracilis
Tantilla hobartsmithi
Tantilla nigriceps
Masticophis taeniatus
Rhinocheilus lecontei
Scincella lateralis
Teiidae (4 species)
Aspidoscelis gularis
Aspidoscelis inornata
Aspidoscelis marmorata
Aspidoscelis tesselata
Xantusiidae (1 species)
Xantusia extorris*
Bogertophis subocularis
Drymarchon melanurus
Lampropeltis alterna
Lampropeltis annulata
Masticophis schotti
Pantherophis bairdi
Pantherophis emoryi
Pituophis catenifer
Pituophis deppei*
Salvadora deserticola
Salvadora grahamiae
Sonora episcopa
October 2019 | Volume 13 | Number 2 | e189
83
Amphib. Reptile Conserv.
The herpetofauna of Coahuila, Mexico
Table 18 (continued). Distribution of herpetofaunal species in Natural Protected Areas of Coahuila, Mexico, based on estimated inclusions.
Abbreviations are as follows: * = species endemic to Mexico; ** = species endemic to Coahuila; and *** = non-native species.
Natural Protected Area
Dipsadidae (4 species)
Diadophis punctatus
Heterodon kennerlyi
Hypsiglena jani
Leptodeira septentrionalis
Elapidae (1 species)
Micrurus tener
Leptotyphlopidae (3 species)
Rena dissecta
Rena dulcis
Rena segrega
Natricidae (7 species)
Nerodia erythrogaster
Nerodia rhombifer
Storeria hidalgoensis*
Thamnophis cyrtopsis
Thamnophis exsul*
Thamnophis marcianus
Thamnophis proximus
Viperidae (9 species)
Agkistrodon contortrix
Crotalus atrox
Crotalus lepidus
Crotalus molossus
Crotalus morulus*
Crotalus ornatus
Crotalus pricei
Crotalus scutulatus
Sistrurus tergeminus
Testudines (11 species)
Emydidae (5 species)
Pseudemys gorzugi
Terrapene coahuila**
Trachemys gaigeae
Trachemys scripta***
Amphib. Reptile Conserv.
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84 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Table 18 (continued). Distribution of herpetofaunal species in Natural Protected Areas of Coahuila, Mexico, based on estimated inclusions.
Abbreviations are as follows: * = species endemic to Mexico; ** = species endemic to Coahuila; and *** = non-native species.
[Kinosteraine @peesy i
[Kinoserion durngoonse®™ —__——*d—
Frestusinidne @specis) i
Trionychidae (2 species)
Apalone atra**
sesoualy oneng
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Of the 120 species included in Table 18, 26 (21.0%) are
endemic species, including seven (5.8%) state endemics
(Gerrhonotus mccoyi, Crotaphytus antiquus, Uma exsul,
Scincella kikaapoa, Terrapene coahuila, Trachemys
taylori, and Apalone atra). Ninety-one of the 120 species
(75.8%) are non-endemics, and three (2.5%) are non-
natives (all of the three that occur in the state). Naturally,
it is not desirable to have the non-native species within
protected areas, but, fortunately, only one of the three
(Hemidactylus turcicus) 1s expected to be found in more
than three of the areas (and it is expected in all of them).
Of the 23 species that are not expected to be found
within the 19 existing protected areas, 12 are country
endemics:
Eleutherodactylus longipes
Rheohyla miotympanum
Ambystoma velasci
Aquiloeurycea galeanae
Aquiloeurycea scandens
Chiropterotriton priscus
Barisia imbricata
Phrynosoma orbiculare
Sceloporus cyanostictus
Sceloporus goldmani
Sceloporus minor
Scincella silvicola
One of the 23 species (Sceloporus gadsdeni) is a state
endemic and 10 are non-endemics (Acris blanchardi,
Smilisca baudinii, Holbrookia lacerata, Sceloporus
Amphib. Reptile Conserv.
85
marmoratus, Lampropeltis gentilis, Tantilla cucullata,
Trimorphodon vilkinsonii, Crotalus viridis, Terrapene
ornata, and Kinosternon hirtipes).
The principal herpetofaunal conservation goal for
Coahuila, at this point, is to conduct herpetofaunal
surveys in all currently-established conservation areas to
determine which species are now actually represented.
Based on this analysis, we predict that relatively few
Species are expected to be absent from all of these 19
areas, So a subsidiary goal is to ascertain whether this 1s
the case and, if so, what other areas could be established
to contain them.
Conclusions and Recommendations
Conclusions
A. At the present time, the herpetofauna of Coahuila
comprises 143 species, including 20 anurans, four
salamanders, 106 squamates, and 13 turtles; three species
are non-natives.
B. The number of herpetofaunal species distributed
among the 10 physiographic regions we recognize in
Coahuila varies from 38 in the Laguna de Mayran region
to 91 in the Sierras y Llanuras Coahuilenses.
C. The level of endemism of the herpetofauna of
Coahuila is relatively low. Of the 143 species recorded
from the state, 40 are endemic to Mexico, including nine
limited to Coahuila. Thus, the percentage of endemism
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
Table 19. Summary of the distributional status of herpetofaunal species in protected areas in Coahuila, Mexico. Totals = total
number of species recorded in all of the listed protected areas.
Protected Areas Number
Los Novillos
Cuenca Alimentadora del Distrito
Nacional de Riego 04 Don Martin
Distrito Nacional de Riego 026 Bajo
36
Rio San Juan.
Rancho Media Luna
Rancho La Puerta
Tierra Silvestre Cafion del Diablo
is 28.6%. The 40 endemic species amount to 4.9% of the
811 endemic species in Mexico.
D. The distributional status of the Coahuilan herpetofauna
is as follows (in order of the size of the categories): non-
endemics (100, 69.9%); country endemics (31, 21.7%);
state endemics (nine, 6.3%); and non-natives (three,
2.1%).
E. The principal environmental threats in Coahuila are
urban development, industrial pollution, deforestation
for agricultural and ranching purposes, road effects,
mining and energy projects, natural gas fracking, wind
turbines, elimination due to cultural beliefs and practices,
collecting and commercial trade, and forest fires.
F. The SEMARNAT, IUCN, and EVS systems were used
to evaluate the conservation status of the herpetofauna
of Coahuila. As demonstrated in previous MCS studies,
the SEMARNAT system proved to be of little value,
inasmuch as only 35.7% of the native herpetofauna
has been evaluated to date. Of these 50 species, four
are placed in the endangered category (P), 23 in the
threatened category (A), and 23 in the special protection
category (Pr).
G. The IUCN system was also applied to assess the native
Coahuilan herpetofauna, and the results (by category
Amphib. Reptile Conserv.
Distributional Status
(NE) Endemic (CE) (SE) (NN)
|RioBravodelNorte | 76 | 8 3
| MaderasdelCarmen | 79TH
and proportion) are: CR (0 of 140 species; 0%); EN (7;
5.0%); VU (7; 5.0%); NT (8; 5.7%); LC (94; 67.1%); DD
(1; 0.7%); and NE (23; 16.4%).
H. In addition, the EVS system was applied to the 140
native Coahuilan species. It placed them in the low,
medium, and high vulnerability categories, and the
values increased from low (33; 23.6%) to medium (55;
39.3%) and then slightly decreased in the high category
(52; 37.1%).
I. The IUCN and EVS conservation status allocations
ascertained that only 26.9% of the EVS high vulnerability
species have been placed in two of the three IUCN
threat categories (EN and VU; while no species are
allocated to the CR category) and only 35.1% of the EVS
low vulnerability species have been placed in the LC
category. As such, the results of the application of these
two systems do not correspond well to one another.
J. An analysis of the conservation status of the 118
species placed in the IUCN DD, NE, and LC categories
demonstrates that many of them have been evaluated
inappropriately compared to their respective EVS values.
We opine that these species need to be reassessed to
better reflect their prospects for survival.
K. The Relative Herpetofaunal Priority (RHP) measure
October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
Fig. 23. Forest Fires. The scene after a forest fire in the vicinity of Arteaga, in the municipality of Arteaga. Photo by Manuel
Nevarez de los Reyes.
was applied to establish the conservation significance
of the ten regional herpetofaunas in Coahuila, which
indicates that the most significant herpetofauna 1s that
of the Gran Sierra Plegada, as it contains the greatest
number of country endemics and the second greatest
number of high vulnerability species. The other nine
physiographic regions are arranged in decreasing order
of significance on the basis of their number of endemic
species, as follows: Sierra Transversales; Sierras y
Llanuras Coahuilenses; Bolson de Mapimi; Pliegues
Saltillo Parras; Laguna de Mayran and Sierra de la Paila;
Llanuras y Sierras Volcanicas, Serranias del Burro, and
Llanuras de Coahuila y Nuevo Leon. On the basis of their
numbers of high vulnerability species, the ranking is as
follows: Sierras y Llanuras Coahuilenses; Gran Sierra
Plegada; Sierras Transversales; Pliegues Saltillo Parras;
Bolson de Mapimi; Llanuras y Sierras Volcanicas and
Serrania del Burro; Laguna de Mayran, Sierra de la Paila,
and Llanuras de Coahuila y Nuevo Leon.
L. Nineteen protected areas have been established in
Coahuila; eight federal reserves, four federal/private
reserves, three state reserves, three state/private reserves,
and one municipal reserve. The representation of these
19 areas among the ten physiographic areas is weighted
in favor of the Sierras y Llanuras Coahuilenses (eight
areas), which ranked 3“ in endemic species and 1* in high
vulnerability species. The Gran Sierra Plegada is the next
best represented (in four areas). Unfortunately, all of the
19 protected areas for which information is available are
occupied by landowners. In addition, few areas have the
Amphib. Reptile Conserv.
87
benefit of herpetofaunal surveys or management plans.
M. Our analyses predict that 120 of 143 total species are
expected to be found in the 19 protected areas (83.9%).
These 120 species include 91 non-endemics, 19 country
endemics, seven state endemics, and three non-natives.
The non-native species should not be included the
protected areas system.
N. Future conservation efforts should be directed
toward conducting thorough herpetofaunal surveys in
all components of the protected areas system, as well as
determining what additional areas might be required to
provide protection for all of Coahuila’s herpetofaunal
species.
Recommendations
A. Our principal interest in writing this paper has
been to assess the conservation status of the 140
native species presently recorded from the state of
Coahuila, and to suggest what steps need to be taken
to protect all of these species over the long term.
We have undertaken this assessment using the EVS
methodology, as we have in the previous entries in the
Mexican Conservation Series, which demonstrated
that 33 species are allocated to the low vulnerability
category, 55 to the medium vulnerability category, and
52 to the high vulnerability category. We also employed
the Relative Herpetofaunal Priority methodology to
determine which of the physiographic regions in the
October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
No. 21. eis Tees (Kennicott, a The ae Rattlesnake is distributed “in the United States in eeouihesstern Arizona,
southern New Mexico, and western Texas” and “in Mexico...in Sonora, Chihuahua, Durango, Sinaloa, Nayarit, Jalisco, Zacatecas,
Aguascalientes, Coahuila, Nuevo Leon, and San Luis Potosi” (Prival and Porter 2016: 444). This individual came from Jimenez,
in the municipality of Jimenez. Wilson et al. (2013a) evaluated its EVS as 12, placing it in the upper portion of the medium
vulnerability category. Its conservation status 1s considered as Least Concern by IUCN and as a species of special protection (Pr) by
SEMARNAT. Photo by Michael S. Price.
NG IAI
No. 22. eee pricei Van Seine: 1895. “The Twin- etn es ranges “from ee ean in the United
States (Chiricahua, Huachuca, Pinaleno, Dos Cabezas, and Santa Rita mountains) southward in Mexico through the Sierra Madre
Occidental to northeastern Sonora, western Chihuahua, and Durango, and in the Sierra Madre Oriental of southeastern Coahuila,
southern Nuevo Leon, southwestern Tamaulipas, and north-central San Luis Potosi, and in Aguascalientes” (Hammerson et al.
2007). This individual was found at Monterreal, in the municipality of Arteaga. Wilson et al. (2013a) assessed its EVS as 14, placing
it at the lower limit of the high vulnerability category. Its conservation status is judged as Least Concern by IUCN and as a species
of special protection (Pr) by SEMARNAT. Photo by Eli Garcia Padilla.
Amphib. Reptile Conserv. 88 October 2019 | Volume 13 | Number 2 | e189
Lazcano et al.
No. 23, Sa eels (Say, 1823). The weston WMastesaea occurs in ihe USA (Texas, Otisnona) and Wiexen (central
and northeastern Coahuila, southern Nuevo Leon; possibly in Tamaulipas, northern Chihuahua, and northeastern Sonora). This
individual came from 6 km south of La Piedra Parada, in the municipality of Guerrero. The EVS value of this rattlesnake is 13. Its
conservation status has not been assessed by IUCN and it is not listed by SEMARNAT. Photo by Manuel Nevarez de los Reyes.
No. 24. Terrapene coahuila Schmidt a Owens, 1944. The Cent BOs Turtle i isa Mena Son species restricted to “the
Cuatro Ciénegas Bolson of Coahuila” (Lemos-Espinal et al. 2015: 122). This individual was located at Cuatrociénegas in the
municipality of Cuatrociénegas de Carranza. Wilson et al. (2013a) calculated its EVS as 19, placing it in the upper portion of the
high vulnerability category. Its conservation status is determined as Endangered by IUCN and as threatened (A) by SEMARNAT.
Photo by Michael S. Price.
Amphib. Reptile Conserv. 89 October 2019 | Volume 13 | Number 2 | e189
The herpetofauna of Coahuila, Mexico
«a
ae
ls te
+
i oa a oe ee Reo A coos eg Lo x | =
No. 25. Zrachemys taylori (Legler, 1960). The Cuatro Ciénegas Slider is an endemic Mexican species restricted in distribution to the
Cuatro Ciénegas Basin (Lemos-Espinal et al. 2015). This individual came from Cuatrociénegas in the municipality of Cuatrociénegas
de Carranza. Wilson et al. (2013a) determined its EVS as 19, placing it in the upper portion of the high vulnerability category. Its
conservation status is calculated as Endangered by IUCN, but this species is not listed by SEMARNAT. Photo by Michael S. Price.
state support the most significant herpetofaunas based
on the relative numbers of country endemics and high
vulnerability species. Three such areas were identified:
the Gran Sierra Plegada, the Sierras Transversales, and
the Sierras y Llanuras Coahuilenses. Fortunately, these
three regions support the greatest numbers of protected
areas among the 19 that are currently established, four,
four, and eight, respectively. The herpetofaunal content
of these protected areas, however, is very poorly known;
as a result, the major conservation goal with respect to
the herpetofauna of Coahuila is to carefully document
the species inhabiting the protected areas of the state in
order to test the predictions made here about their content
and to draw up adequate management plans for their
perpetual protection.
B. Thus, it will only be after the species inhabiting
the existing protected areas have been identified that
additional conservation goals can be addressed. These
goals include (1) determining what other protected areas
might need to be established to protect the remainder of
the herpetofauna not found within the existing areas, (2)
monitoring of the health of the populations of species
within the protected areas, and (3) assessing the well-
being of the ecosystems on which these species depend.
C. It is imperative that this work advance as rapidly
as possible, especially given that efforts to protect
Amphib. Reptile Conserv.
the Coahuilan herpetofauna lag behind those of the
other Mexican states examined thus far in the Mexican
Conservation Series.
“We have come a very long way through the barbaric
period in which we still live, and now I believe we have
learned enough to adopt a transcendent moral precept
concerning the rest of life. It is simple and easy to say:
Do no further harm to the biosphere.” —E.O. Wilson
(2016)
Acknowledgments.—We are very thankful to those
individuals who allowed us to use their outstanding
photographic images of many of the amphibians,
reptiles, ecosystems and environmental issues illustrated
in this paper, including: Michael S. Price; Marco Antonio
Bazan-Tellez; Uri Garcia- Vazquez; Daniel Garza Tobon;
Bernardo Marino (http://gransierraplegada.org); Gabriel
Viesca Ramos; José Flores Ventura; and Daniel Solorio
Estrada. We are indebted to Dr. José Juan Flores from
Especies, Sociedad y Habitat A. C., for constructing the
physiographic map.
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Amphib. Reptile Conserv.
Lazcano et al.
David Lazcano is a herpetologist who earned a bachelor’s degree in chemical science in
1980, and a bachelor’s degree in biology in 1982. In 1999, David earned a master’s degree
in wildlife management, and a doctoral degree in biological sciences with a specialty
in wildlife management (2005), all from the Facultad de Ciencias Bioldgicas of the
Universidad Autonoma de Nuevo Leén (UANL). Currently, he is a full-time professor
j at the same institution, where he teaches courses in animal behavior, biogeography,
biology of chordates, and wildlife management. David is also the head of Laboratorio
de Herpetologia and Coordinacion de Intercambio Académico de la Facultad de Ciencias
Biolégicas at UANL. Since 1979, he has been teaching and providing assistance in
both undergraduate and graduate programs. David’s research interests include the
, herpetofaunal diversity of northeastern Mexico, as well as ecology, herpetology, biology
of the chordates, biogeography, animal behavior, and population maintenance techniques
of montane herpetofauna.
Manuel Nevarez-de los Reyes is a biologist who graduated from the Universidad
Autonoma de Nuevo Leon (UANL), Facultad de Ciencias Biologicas in San Nicolas
de los Garza, México. Manuel’s initial interest was in the study of amphibians and
reptiles, but his professional life led him to investigate other areas, such as environmental
impacts and the study of cacti. From 1997 to 2007, he served as head of Environmental
Protection in the Residencia Regional de Construccion Noreste of the Federal Electricity
Commission. Manuel has been involved with numerous workshops and conferences, and
has authored both popular science and peer-reviewed articles on herpetology and cacti.
Among his accomplishments, he discovered and co-authored the original description of
a new genus and species of cactus, Digitostigma caput-medusae. The following year he
created “Proyecto Digitostigma,” a nursery dedicated to the commercial propagation of
various cacti, which contributes to their knowledge and conservation. Manuel recently
obtained his Ph.D. in Wildlife Management and Sustainable Development at the UANL,
with a thesis entitled “Ecological distribution of the herpetofauna of the Sierra de Gomas
in northern Nuevo Leon,” under a grant from the National Council of Science and
Technology. He is now part of the herpetological group that has documented the many
herpetological activities in northeastern México (Coahuila, Nuevo Léon, and Estado de
México).
Eli Garcia-Padilla is a herpetologist primarily focused on the ecology and natural history
of the Mexican herpetofauna. His research efforts have centered on the Mexican states
of Baja California, Tamaulipas, Chiapas, and Oaxaca. His first experience in the field
was studying the ecology of the insular endemic populations of the rattlesnakes Crotalus
catalinensis, C. muertensis (C. pyrrhus), and C. tortugensis (C. atrox) in the Gulf of
California. Eli’s Bachelor’s thesis was on the ecology of C. muertensis (C. pyrrhus) on
Isla El Muerto, Baja California, Mexico. To date, he has authored or co-authored over
100 contributions to science. Eli is currently a formal Curator of Amphibians and Reptiles
from Mexico in the electronic platform “Naturalista” of the Comision Nacional para el
Uso y Conocimiento de la Biodiversidad (CONABIO-inaturalist; http://www.naturalista.
mx). One of his main passions is environmental education, and for several years he has
worked on various projects that include the use of photography and audiovisual media as a
powerful tool for reaching large audiences and promoting the knowledge, protection, and
conservation of Mexican biodiversity. Eli’s interests include wildlife and conservation
photography, and his art has been published in several scientific, artistic, and educational
books, magazines, and websites. Presently, he is collaborating on an evaluation of the
jaguar (Panthera onca) as an umbrella species for the conservation of the herpetofauna of
Nuclear Central America.
Jerry D. Johnson is Professor of Biological Sciences at The University of Texas at El
Paso (UTEP), and has been investigating the systematics, ecology, and conservation of
the herpetofauna of Middle America since 1970, especially that of southern Mexico.
Jerry is also the Director of UTEP’s 40,000-acre Indio Mountains Research Station in
the Chihuahuan Desert of Trans-Pecos, Texas. He has authored or co-authored over 120
peer-reviewed papers, and was co-editor or contributor to several major Mesoamerican
herpetology books: Conservation of Mesoamerican Amphibians and_ Reptiles,
Mesoamerican Herpetology: Systematics, Zoogeography, and Conservation, and Middle
American Herpetology: A Bibliographic Checklist. One species, Tantilla johnsoni, was
named in his honor. Presently, Jerry is an Associate Editor and Co-chair of the Taxonomic
Board of the Mesoamerican Herpetology website.
93 October 2019 | Volume 13 | Number 2 | e189
Amphib. Reptile Conserv.
The herpetofauna of Coahuila, Mexico
Vicente Mata-Silva is a herpetologist originally from Rio Grande, Oaxaca, Mexico.
His interests include ecology, conservation, natural history, and biogeography of the
herpetofaunas of Mexico, Central America, and the southwestern United States. Vicente
received his B.S. degree from the Universidad Nacional Autonoma de México (UNAM),
and his M.S. and Ph.D. degrees from the University of Texas at El Paso (UTEP). Vicente
is an Assistant Professor of Biological Sciences at UTEP in the Ecology and Evolutionary
Biology Program, and Assistant Director of UTEP’s 40,000 acre Indio Mountains Research
Station, located in the Chihuahuan Desert of Trans-Pecos, Texas. To date, Vicente has
authored or co-authored over 100 peer-reviewed scientific publications. He also was the
Distribution Notes Section Editor for the journal Mesoamerican Herpetology.
Dominic L. DeSantis is currently a Ph.D. candidate and National Science Foundation
Graduate Research Fellow at the University of Texas at El Paso. He received his Bachelor’s
degree at Texas State University, where he also completed multiple research projects on the
antipredator behavior of the critically endangered Barton Springs Salamander (Eurycea
sosorum). Dominic’s ongoing dissertation research integrates multiple field monitoring
technologies to study snake movement and behavioral ecology. Dominic accompanied
Vicente Mata-Silva, Eli Garcia-Padilla, and Larry David Wilson on survey and collecting
trips to Oaxaca in 2015, 2016, and 2017, and he is a co-author on numerous natural history
publications produced from those visits.
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica. He was
born in Taylorville, Illinois, USA, and received his university education at the University
of Illinois at Champaign-Urbana (B.S. degree) and at Louisiana State University in
Baton Rouge (M.S. and Ph.D. degrees). He has authored or co-authored over 410 peer-
reviewed papers and books on herpetology. Larry was the senior editor or author of several
books, including Conservation of Mesoamerican Amphibians and Reptiles, The Snakes of
Honduras, Middle American Herpetology, The Amphibians of Honduras, Amphibians &
Reptiles of the Bay Islands and Cayos Cochinos, Honduras, The Amphibians and Reptiles
of the Honduran Mosquitia, and Guide to the Amphibians & Reptiles of Cusuco National
Park, Honduras. To date, he has authored or co-authored the descriptions of 72 currently
recognized herpetofaunal species, and seven species have been named in his honor,
including the anuran Craugastor lauraster, the lizard Norops wilsoni, and the snakes
Oxybelis wilsoni, Myriopholis wilsoni, and Cerrophidion wilsoni. Larry previously served
an Associate Editor and is presently Co-chair of the Taxonomic Board for the journal
Mesoamerican Herpetology.
94 October 2019 | Volume 13 | Number 2 | e189
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 95-101 (e190).
Unpublished population data of Dendrobates azureus
Hoogmoed 1969 obtained in 1968 and 1970, and its historical
and current taxonomic status
Marinus S. Hoogmoed
Museu Paraense Emilio Goeldi, Caixa Postal 399, 66017—-970 Belém, Pard, BRAZIL
Abstract.—During a herpetological inventory in the Sipaliwini area in southern Suriname in 1968, and again
during a second expedition to the area in 1970, anecdotal population data on Dendrobates azureus Hoogmoed,
1969 were obtained. As of now, some 50 years later, these data have not been published, yet they may be useful
for the evaluation of the status of this taxon at the present time and the evolution of its populations over the
period since 1968. Visits to the Sipaliwini savanna to observe or collect this taxon over the past 50 years have
been few and far between. An overview of the population data available in the publications about these visits
is provided.
Keywords. Dendrobates tinctorius, isolated populations, Sipaliwini savanna, Suriname, conservation, threats.
Citation: Hoogmoed MS. 2019. Unpublished population data of Dendrobates azureus Hoogmoed 1969 obtained in 1968 and 1970, and its historical
and current taxonomic status. Amphibian & Reptile Conservation 13(2) [General Section]: 95-101 (e190).
Copyright: © 2019 Hoogmoed. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 14 March 2018; Accepted: 10 September 2019; Published: 9 October 2019.
Introduction it seems timely to publish the basic population data of
this taxon, even though they were collected anecdotally.
During a herpetological inventory of the Sipaliwini area Polder (1974), based on his observations of the taxon
in 1968 Hoogmoed (1969a,b, 1971a,b, 1972) discovered __in captivity, expressed some doubt on the specific status
a blue Dendrobatid frog in forest islands in the Sipaliwinit of D. azureus, but this had no direct consequences as
savanna, near the Vier Gebroeders Mountain close to the — Silverstone (1975) considered it a species. Wollenberg
Suriname-Brazilian border, that he named Dendrobates et al. (2006), followed by Wollenberg (2007), on the
azureus. In the description (Hoogmoed 1969b),a number basis of morphological data and genetic analysis,
of ecological and behavioral data were provided, but synonymized D. azureus with D. tinctorius (Cuvier,
data that give an impression about the abundance of the 1797). This assessment was supported by Noonan
population were not presented, because they were not and Gaucher (2006), who found that specimens of D.
collected in a systematic way, but rather anecdotally. azureus (from the type locality or near to it, see below,
The author paid a second visit to the Sipaliwini area and Noonan, pers. comm.) shared the same haplotype with
the habitat of D. azureus in 1970 (Hoogmoed 1971a,b, _ two “nearby” (from the continuous rainforest, see below,
1972) and more data were obtained on the abundance = Noonan, pers. comm.) populations of D. tinctorius and
of the frog in the type locality (forest island on West — concluded that this signified the two taxa were identical.
slope Vier Gebroeders Mountain) and some other forest Grant et al. (2006) still treated D. azureus as a species
islands nearby, and about forest island occupation by this —_ but on the basis of molecular results were inclined to
taxon. These population data are available inthe author’s _— follow the synonymy suggested by Wollenberg et al.
field books (archived in the former Rijksmuseum van = (2006). Gaucher and McCulloch (2010) and Frost (2018)
Natuurlijke Historie, now Naturalis Biodiversity Center accepted the synonymization and considered D. azureus
in Leiden [RMNH], in the Netherlands) and in his private — a synonym of D. tinctorius. Ouboter and Jairam (2012)
diary notes, and they can provide basic data about the considered D. azureus a subspecies of D. tinctorius,
population status of the taxon at the time of its discovery. —_ without providing arguments, but this was not accepted
This taxon is considered vulnerable [VU: D2] (Stuart et by Frost (2018), who treated D. tinctorius as monotypic.
al. 2006), and as a member of the genus Dendrobates it is However, Avila-Pires et al. (2010) and Hoogmoed
on CITES Appendix II, so in Suriname it officially cannot —_ (2013) did not accept the synonymization by Wollenberg
be traded (Hoogmoed 2013). However, since it still has et al. (2006) and pointed out that this publication suffered
been subject to illegal capture and export of specimens, several shortcomings. Here I add to those critiques the
Correspondence. marinus@museu-goeldi.br
Amphib. Reptile Conserv. 95 October 2019 | Volume 13 | Number 2 | e190
Dendrobates azureus in Suriname 1968-1970
use of tissue samples of captive bred material of dubious
origin (although stated to be from the type locality) and
the fact that among dendrobatid breeders D. azureus has
been confused with, and interbred with, a blue morph of D.
tinctorius that occurs in southern Guyana, northwestern
Para in Brazil (south to Porto Trombetas) and possibly
in extreme southwestern Suriname (in a contested area
between Suriname and Guyana). See Avila-Pires et al
(2010: Fig. 23) and Lotters et al. (2007: Fig. 707) for
color pictures of this blue D. tinctorius morph. Hoogmoed
(1969, 2013: Fig. 4), Eisenberg (2004), and Lotters et al.
(2007: Fig. 708 [as D. tinctorius|) provide pictures of D.
azureus. Noonan and Gaucher (2006) mention specimens
of D. tinctorius and D. azureus from slightly different
localities (Table 1) and their samples of D. azureus are
from the area of Vier Gebroeders Mountain (see Noonan,
pers. comm., below as well). In Wollenberg et al. (2008) it
seems that the blue morph of D. tinctorius has incorrectly
been considered as D. azureus (see Fig. 4 Haplotype 2,
the second figure from above and the lower figure; no
D. azureus can be found in this figure). Unfortunately,
only the fancy names of hobbyists have been used for
the “Sipaliwini” material and no vouchers have been
indicated.
In order to remove any doubt regarding which
population I am discussing, and avoid upsetting the
present accepted nomenclature, below I use the name
Dendrobates “azureus” in the sense of the population of
D. tinctorius described in 1969 as D. azureus and only
known from isolated forest islands in the Sipaliwini
savanna in southern Suriname.
History of (the herpetological) exploration of
the Sipaliwini Savanna and inventories of D.
“azureus” populations
1935-1938: Border expedition (van Lynden 1939)
to establish the border between Suriname and Brazil
(= watershed). Although Van Lynden stayed on the
Sipaliwini savanna for an extended period (4 October
1935 to 10 March 1936), and made general observations
about animals (mostly mammals and birds), he did not
mention “blue frogs,” so we may conclude he did not
observe them, or that he did not deem them worthy of
mentioning. His camp III (on the western base of Vier
Gebroeders Mountain, from where he wrote his diary
on 12 October 1935) actually was close to the later
type locality of D. “azureus,” but it was probably in the
savanna itself, not in the forest island. The map published
by van Lynden (1939) unfortunately does not show the
location of the forest islands.
1961: During Operation Grasshopper, the Sipaliwini
airstrip was constructed on a small savanna about 3.5
km west of the western border of the Sipaliwini savanna.
Apparently, the forest islands in the savanna were not
visited.
1968: Hoogmoed (1969a,b) discovered populations of
D. “azureus” in four forest islands in the middle of the
Sipaliwini savanna near the Vier Gebroeders Mountain
Amphib. Reptile Conserv.
Fig. 1. Dendrobates “azureus” (= tinctorius).
when making a herpetological inventory of the area in
1968 (22 August to 7 October), concentrating on the
area between Sipaliwini airstrip and Vier Gebroeders
Mountain. He collected a total of 37 specimens and
two tadpoles of D. “azureus” (Table 1), which were all
preserved and form the type material of the description of
D. azureus Hoogmoed, 1969. The location and shape of
the forest islands as shown in Hoogmoed (1969b: Fig. 3)
were taken from a topographical map (Centraal Bureau
Luchtkartering, Paramaribo, Suriname) of the area based
on aerial photographs.
1968-1969: After Hoogmoed’s departure from the area,
the Sipaliwini expedition (Hoogmoed 1969a) continued
working in the Sipaliwini savanna and the participants
(botanists and a geologist) moved N of the Vier
Gebroeders area to the Morro Grande Mountain area.
Hoogmoed (1969b: Fig. 3) marked four northern forest
islands as possible localities for D. “azureus” because
the botanist J.P. Schulz reported having seen “blue frogs”
there. Considering later observations (see Gagliardo 2004
a,b; Fouquet et al. 2015), these might well have been D.
tinctorius with a yellow semicircular mark on the snout.
1970: Between 13 January and 13 February Hoogmoed
again visited the Sipaliwini savanna, this time
concentrating on the part south of the Vier Gebroeders
Mountain and the Brazilian border. During this trip one
specimen of D. “azureus” was collected and preserved,
and 10 additional specimens were collected at the type
locality and transported alive to the Netherlands, where
they were bred in captivity by Polder (1973a-—c, 1974).
1981: According to Wevers (2007), a “group of
Dutchmen” brought live D. “azureus” from the Sipaliwini
savanna (most likely an illegal operation), making no
mention of the names of participants, numbers of frogs
brought back, or from which forest island(s).
1988: An illegal import of D. “azureus” (apparently
three specimens) was confiscated in the Netherlands and
transferred to Blijdorp Zoo, Rotterdam (Wevers 2007).
1996: Cover (1996, 1997) reported on an expedition
in June 1996 (sponsored by the National Aquarium in
Baltimore, USA) to attempt a population survey of D.
October 2019 | Volume 13 | Number 2 | e190
Hoogmoed
Table 1. Detailed data for specimens of D. “azureus” collected/observed by M.S. Hoogmoed in 1968 and 1970. Number of
specimens accounts for both collected and observed specimens, numbers between brackets in the first column refer to the numbers
of forest islands as used in the text. The asterisk (*) indicates that 10 specimens were observed in about 10 minutes.
Forest
island Number of specimens | Time spent in field
(see text)
Person-minutes Number person-
spent in field minutes per specimen
1968
5 (+ 2 spol
au GUN BE) — ——
23 Sep 10 ——— coll, RMN a 00-11:00 h
a
=a Mean or total
1970
A CT ——
Soa eae
Total 1968 + 1970
82 (38 preserved, 10
live for ex situ breeding
colony)
“azureus.” Three staff members of the NAIB and three _— (and finally exported) in a forest island northeast of the
field workers of Conservation International Suriname Sipaliwini airstrip. One day before departure from the
participated. Fifty-four adults and two juveniles were = savanna permission was obtained to collect and export
observed during a limited number of days. They surveyed 20 specimens of D. “azureus,” so they had to be collected
six forest islands and found specimens in three of them at arush and were meant to establish an ex-situ breeding
“two on the slopes of Vier Gebroeders and one ina valley —_ population (Eiben 2005). No mention was made of which
floor forest just north of the mountains” (Cover 1997; forest island(s) these specimens were collected from or
Eiben 2005). Most likely Cover referred to forest island |= how much time it took to collect them.
nos. 1 and 4 on the slopes of Vier Gebroeders Mountain
and to forest island no. 2 north of that mountain (see 2003: B.P. Noonan (pers. comm.; Eiben 2005) visited
below). No material was collected, and the position of — the area of the Vier Gebroeders Mountain from 23—26
the other three forest islands was not mentioned. May 2003. He flew in using Mamiya airstrip (= “Myers’
airstrip” in Hoogmoed (1969) and in the present text,
1997: Gagliardo (2004a,b) reported on a new expedition Wapaisana Anotato on Google Earth) on the border
(14 August-19 September 1997) by Cover and three of Suriname and Brazil, SE of the Vier Gebroeders
other zoo curators in order to collect specimens to Mountain, and he left via Sipaliwini airstrip, W of the
establish a breeding population in the USA. “Nearly 60 — savanna. He was not allowed to collect specimens of D.
specimens” and an unknown number of tadpoles were “azureus,” but was allowed to make toe clips from 10
observed in two forest islands that were not the type — specimens for molecular studies (Noonan and Gaucher
locality. Furthermore, three pairs of D. tinctorius (witha 2006). He found three specimens on 24 May, four
yellow semi-circular mark on the snout) were collected = specimens on 25 May, and another three on 26 May. No
Amphib. Reptile Conserv. 97 October 2019 | Volume 13 | Number 2 | e190
Dendrobates azureus in Suriname 1968-1970
data on time spent finding specimens are available, but
Noonan writes: “....my experience was that neither of
these populations was terribly dense. While I did not
keep detailed notes on abundance, I am comfortable
saying that I did not observe more than one individual per
hour of searching (on average).” Noonan also collected
tissue from three Dendrobates specimens found in the
continuous rainforest NE of the airstrip Sipaliwini, about
100 m from the savanna edge, that were identified as D.
tinctorius (Noonan and Gaucher 2006).
2007: According to Wevers (2007) several frog fanciers
visited the Sipaliwini savanna and “observed respectively
9, 15 [probably Wevers himself] and 20 specimens
(mostly the same specimens).” Wevers (2007) visited the
Sipaliwini savanna for five days in February and during
those days observed 15 specimens and four larvae. He
at least visited the type locality on the western slope of
the Vier Gebroeders Mountain and the forest island on
the northeastern slope from where he reported juvenile
specimens. He reported that his guide who lived on
Mamiya airstrip (= “Myers’ airstrip”) on the frontier of
Suriname and Brazil, never had seen more than 25 D.
“azureus”’ in one day. Based on his own observations
(five days and a limited number of forest islands visited)
and information from his Indian guides, he estimated
the size of the total wild population to be between 1,000
and 1,500 specimens, but this does not seem to be a very
reliable figure.
2014: Fouquet et al. (2015) visited the Sipaliwini area
between 15 and 28 April, but did not visit the forest
islands where D. “azureus” occurs. They reported D.
tinctorius (with a yellow semi-circular mark on the
snout) from a mountain 10 km N of Sipaliwini airstrip in
the area of continuous rainforest.
By no means is this overview intended to be an
exhaustive listing of all visits to the D. “azureus” habitat
or nearby areas. It is known that Suriname scientists
with a license to study the frogs and personnel of the
Forestry Service flew into Sipaliwini airstrip, but were
not allowed to travel from there to the Vier Gebroeders
Mountain and they were confined to the airstrip. Some
scientist may have paid unregistered (and unpublished)
visits to the area. Illegal collectors (animal dealers) and
terrarium keepers apparently have visited the area at
least several times, but because of the nature of these
trips, they have not been documented publicly. It also is
possible that native and Brazilian Indian collectors have
provided animal dealers with specimens that may have
left Suriname directly or via Brazil. No numerical data
are available, but Suriname animal dealers exporting
reptiles and amphibians to the USA and Europe have
long-standing commercial contacts (since the early
1970’s) with the Indians of the villages of Alalapadu and
Kwamalasemutu.
Material and Methods
During the 1968 herpetological inventory of the Sipaliwini
savanna in southern Suriname (Hoogmoed 1969a,b), five
forest islands near the Vier Gebroeders Mountain were
Amphib. Reptile Conserv.
searched. In 1970, Hoogmoed surveyed five forest islands
in the southern part of the savanna. During the fieldwork
in the area around Vier Gebroeders Mountain no formal
population surveys were made, but notes were kept about
how many specimens were observed/collected during
the time spent along transects in the forest islands. Frogs
were observed/collected while traversing forest islands
following creek beds, either downhill or ascending the
creek, generally searching an area of five m at each side
of the stream. The time period during which frogs were
collected was noted, and based on this the abundance
was expressed in specimens per person-minutes. In 1968
observations/collections were made by one person, and
in 1970 by two people. All specimens were either simply
observed, or collected by hand. Specimens collected were
killed with MS222, fixed and preserved in 70% ethanol
(thus, no formaldehyde was used and the type specimens
could still be used for DNA analysis). Live specimens were
transported in plastic bags with leaf litter, and termites
were provided as food.
Data on specimens collected in 1968 were provided
by Hoogmoed (1969b) in general terms. The coordinates
of forest islands where D. “azureus’” was found were
calculated in 1968 on the basis of a topographic map of
the area, but they now can be provided more precisely,
based on localization with Google maps. Only slight
differences can be noticed.
In 1968, the area of the Sipaliwini savanna where
D. “azureus” was obtained was visited between 11
September and 1 October, a total of 21 days. During
this period, several forest islands on and near the Vier
Gebroeders Mountain (as well as the intervening savanna
area) were searched for herpetofauna. Coordinates for
the center of the forest islands are given as in Hoogmoed
(1969b) and corrected according to Google Earth 2018,
datum W84. Forest islands inhabited by D. “azureus” are
indicated with asterisks (*).
1. *Forest island W flank Vier Gebroeders Mountain
(Base Bivouac), type locality of D. azureus,
2°N, 55°58’W (corrected to 2°00’21.24°N,
55°58°10.85”W)
2. *Forest island (J-shaped [the eastern narrow
extension is not rainforest but gallery forest of
Manritia palms]) 1.5 km NE of Vier Gebroeders
Mountain, 2°01’N, 55°57.30’W (corrected to
2°00’59.30”N, 55°57’ 26.03” W)
3. *Forest-island 2 km (note this distance differs
from that in the description of D. azureus) N of
Vier Gebroeders Mountain, long and narrow,
directed W—-E, 2°01’N, 55°58’W (corrected to
2°01°25.78"N, 55°57’°34.22”W)
4. *Forest island on NE slope Vier Gebroeders
Mountain, 2°N, 55°57’30"W (corrected to:
2°00’24.92”N, 55°57’ 22.03” W)
5. Forest island (small) on N slope Vier Gebroeders
Mountain (Google Earth 2°007°52.49"N,
55°58’°04.71”W)
In 1970, the Sipaliwini savanna was visited again (13
January—13 February), this time mostly in a part further
south from the area visited in 1968, with a stay of only
October 2019 | Volume 13 | Number 2 | e190
Hoogmoed
two days in forest island no. 1 (see above). During this
period the following forest islands, that turned out not to
be inhabited by D. “azureus,” were searched (coordinates
based on Google Earth 2018):
6. Small forest island on northernmost part of Lange
Dijk, 2°00’09.36”N, 55°55’°58.78”W, Suriname,
27 January 1970
Small forest island on ridge of Lange Dijk,
1°59°28.01”"N, 55°55715.81”W, Brazil, 27
January 1970
Elongate forest island on SW slope Lange Dijk,
1°59°18.74"N, 55°55’20.73”W, Brazil, 27
January 1970
Westernmost small forest island of two, E
of Myers’ farm, about 8 km WSW of Vier
Gebroeders Mountain W flank, 1°59’°09.10’N,
56°02’35.11”W, Suriname, 4 February 1970
Easternmost (630 m E of and twice as large as
no. 9) forest island, E. of Myers’ farm, about 8
km WSW of Vier Gebroeders Mountain W flank,
1°59°11.78"N, 56°02713.63”W, Suriname, 4
February 1970.
10.
Results
Forest Islands
The shapes and sizes of eight forest islands in 1968 were
based on a topographical map and aerial photographs
that formed the basis for Figure 3 in Hoogmoed (1969b).
These were all compared with Google Earth images of 31
December 1969 and 17 November 2004 (the most recent
freely available large-scale images on the Internet), and
all the forest islands still exist and no notable changes
in shape or size were observed. Cover (1997) noted that
concern had been expressed that the anthropogenic fires
which ravage the savanna yearly might damage the forest
islands. In 1970, Hoogmoed observed that savanna fire
had destroyed the narrow band of forest between the
1968 Vier Gebroeders Bivouac (type locality) and the
savanna on the SW edge of the campground, but also
that the forest island interior, probably because it 1s
rather moist, had not suffered any damage. D. “azureus”
was still regularly present in the former, open camp
ground. Gagliardi (2004a,b) stated that the fires did enter
the forest islands, but he did not mention the extent of
damage. Wevers (2007) wrote that fire had gnawed at the
edges of the forest islands and expressed fear that in an El
Nifio year fire might reach the interior of the forest islands
and thus threaten their integrity. Cover (1997), however,
reported that the fires apparently did not damage the
forest islands, but thought that they might be the reason
that the forest islands did not expand into the savanna.
These last observations are confirmed by Hoogmoed’s
1970 observations (Hoogmoed 1972) and by the Google
Earth images of 2004. The Map for Environment (2018)
shows that there has been only limited tree loss in the
Sipaliwini savanna between 2000 and 2014, although
tree loss near Sipaliwini airstrip has been significant. The
forest islands themselves do not show any noticeable
changes.
Amphib. Reptile Conserv.
99
The most recent Google Earth images (2004) show
that in the Brazilian part of the savanna (Paru savanna)
south and east of the Sipaliwini savanna there are six
large forest islands that would be worth investigating
for the presence of D. “azureus.” However, as this area
is a Brazilian Indian Territory, conducting biological
research there is very difficult, because of the need for
special permits and its remoteness. Just south of the Paru
savanna in Brazil is another, isolated, more or less oval
savanna with a large, elongate forest island in the middle
(160 km SSW of Sipaliwini airstrip). This forest island
was inventoried by Avila-Pires et al. (2010: ESEC Grao
Para Centro) and they did not find any Dendrobates
species there.
Population Data
11 September—1 October 1968. For this period of 21
days spent in Vier Gebroeders Bivouac, general herpe-
tological collecting was conducted in the savanna and
forest islands on and near Vier Gebroeders Mountain.
Only some parts of the days were spent in forest islands
searching for D. “azureus.”
Apart from the four forest islands where specimens
were observed and collected, one small forest island on
the N slope of Vier Gebroeders Mountain was searched
for D. “azureus,” but no specimens were found. The four
northernmost forest islands in Hoogmoed’s (1969) map
were not visited during this time. Data on time spent ob-
serving/collecting D. “azureus” and population density
are summarized in Table 1.
Between 1968 and 1970. The population density of D.
“azureus’ in forest island no. 1 on the W slope of the Vier
Gebroeders Mountain seems to have diminished consid-
erably (remembering that 23 specimens and two tadpoles
were removed in 1968, which might have had a negative
influence on the population), viz. one specimen per 4.7
person-minutes in 1968 (one observer only), versus one
specimen per 19.2 person-minutes in 1970 (two observ-
ers).
In 1970 an additional 11 specimens were removed
from this same forest island, one for the RMNH collec-
tion, and ten live specimens to establish an ex-situ breed-
ing colony in the Netherlands.
It should be mentioned that specimens were not even-
ly distributed throughout the forest islands. They might
be absent in certain stretches and be numerous in other
parts (generally near creeks and/or in areas with large
boulders).
No comparative data for the other forest-islands are
available for the period 1968-1970. Cover (1996, 1997)
does not provide data in a comparable way, but he ap-
parently collected data in three of the forest islands men-
tioned by Hoogmoed (1969), but unfortunately the lo-
cations of these have not been published. Noonan (pers.
comm. 2017) reported that he did not see more than one
specimen per hour. Already in 1968, the population den-
October 2019 | Volume 13 | Number 2 | e190
Dendrobates azureus in Suriname 1968-1970
sity in the other forest islands seemed to be less (one
specimen per 18—30 person-minutes) than in the largest
forest island (no. 1) on the W slope of Vier Gebroeders
Mountain (one specimen per 4.7 person-minutes). This
could be related to the size of the forest islands, but this
is Just an impression that is not based on firm facts. Also,
we have to take into account that more time was spent in
forest island no 1, because it was the location of the camp
(both in 1968 and 1970).
Collections in 1968 were made during the second part
of September, during the dry season, and those in 1970
were made in early February, during the beginning of the
wet season—when rainfall is about twice that in the dry
season, and about half that of May and June, the wettest
months (see Hoogmoed 1969).
Conclusions
At the time of the discovery of D. “azureus” in 1968
it was clear that not all forest islands inhabited by this
taxon had populations of the same density. Since 1968,
although several expeditions have visited the distribution
area of D. “azureus” in the Sipaliwini savanna, no
data on population densities have been published that
could be directly compared with those presented here.
However, the anecdotal data available (see the History
of ... inventories of D. “azureus” populations section
above) give the strong impression that the numbers of
D. “azureus” in its restricted habitat have considerably
diminished since 1968. This impression should be
confirmed by systematic population studies that might
serve in situ and ex situ management programs for this
unique population of brilliant blue poison frogs. At the
moment we do not even have an idea about the size of
the population in the wild, but it might run only into the
hundreds. Eiben (2005) and Stuart et al. (2008) described
the successful ex situ breeding program in the National
Aquarium in Baltimore (Maryland, USA) based on 20
specimens collected in 1997 (see above) and some
additional exchanged specimens. This program should
be continued and fortified with the help of the Suriname
authorities and several nature conservation interest
groups, such as WWE, The Nature Conservancy, and
Conservation International, that are already active in
Suriname.
Although the habitat of this taxon 1s completely within
a Suriname Nature Reserve, the area is easily accessible
from Brazil and the border is not patrolled. Illegal visits
by collectors cannot be ignored, and should be taken into
account when making an in situ management plan. Stuart
et al. (2008: 228) optimistically assumed that interest in
wild collected specimens would diminish with successful
breeding in captivity, but this is a naive assumption (e.g.,
IUCN 2015).
Acknowledgements.—Trips to the Sipaliwini savanna
were made in close cooperation with the Suriname
Forest Service (Dienst’s Landsbosbeheer, F. Bubberman,
J.P. Schulz), which supplied laborers and equipment.
Fieldwork in 1968 was funded by a grant (WR 956—
2) from WOTRO (Netherlands Foundation for the
Amphib. Reptile Conserv.
Advancement of Tropical Research). Fieldwork in 1970
was supported by grants from the Foundation Jan Joost
ter Pelkwijk and the legacy of Miss A.M. Buitendijk,
both administrated by the Rijksmuseum van Natuurlijke
Historie, Leiden, Netherlands.
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trip in Suriname in 1968. Zoologische Mededelingen
44(4): 47-73.
Hoogmoed MS. 1969b. Notes on the herpetofauna
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Hoogmoed
of Suriname III. — A new species of Dendrobates
(Amphibia: Salientia: Dendrobatidae) from Suriname.
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4,425-4,435.
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E.J. Brill, Leiden, Netherlands. 376 p.
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gevangenschap van Dendrobates azureus en enkele
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Polder WN. 1973b. Over verzorging en voortplanting in
gevangenschap van Dendrobates azureus en enkele
andere Dendrobatidae (2). Het Aquarium 44(7): 186—
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gevangenschap van Dendrobates azureus en enkele
andere Dendrobatidae (III). Het Aquarium 44(12):
324-330.
Polder WN. 1974. Over verzorging en voortplanting in
gevangenschap van Dendrobates azureus en enkele
andere Dendrobatidae IV. Het Aquarium 45(5): 122—
128.
Silverstone PA. 1975. A revision of the poison-arrow
frogs of the genus Dendrobates Wagler. Natural
History Museum Los Angeles County Science Bulletin
21: 1-55.
Stuart SN, Hoffmann M, Chanson JS, Cox NA,
Berridge RJ, Ramani P, Young BE. 2006. Threatened
Amphibians of the World. Lynx Editions, Barcelona,
Spain; IUCN, Gland, Switzerland; Conservation
International, Arlington, Virginia, USA; NatureServe,
Costa Rica. 758 p.
Wevers E. 2007. In het biotoop van de Okopipi. Onder
het Palmblad 10: 14—23.
Wollenberg KC, Veith M, Noonan BP, Lotters S. 2006.
Polymorphism versus species richness—Systematics
of large Dendrobates from the Eastern Guiana Shield
(Amphibia: Dendrobatidae). Copeia 2006(4): 623-—
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Wollenberg C. 2007. Dendrobates tinctorius —
Polymorphismus oder Artenreichtum? Aquaristik
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2
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poison frog species. Biological Journal of the Linnean
Society 93: 433-444.
Marinus Steven Hoogmoed was curator of Herpetology at the Dutch
National Museum of Natural History (RMNH) in Leiden from 1966
to 2004, and Head of its Department of Vertebrates from 1991 to 2001.
» Marinus obtained his doctorate degree in Mathematics and Natural
~ Sciences at Leiden University, Netherlands, in 1973 based on a monograph
2 of the lizards and amphisbaenians of Suriname. He worked mainly on
systematics, taxonomy, and biogeography of Amazonian and Guianan
® herpetofauna; and he has done fieldwork in all Amazonian countries, except
Guyana. Marinus spent a total of three years in the field in Suriname. After
his retirement, Marinus continued his research in the Amazon area as a
volunteer at the Museu Paraense Emilio Goeldi (MPEG) in Belém, Para,
Brazil, where he is still active. Between 1975 and 2004 he was involved in
CITES as a representative of the Netherlands, and between 2000 and 2002
Marinus was chair of the Animals Committee of CITES.
October 2019 | Volume 13 | Number 2 | e190
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 102-114 (e191).
a
ge
Vulnerability of Northern Pine Snakes (Pituophis
melanoleucus Daudin, 1803) during fall den ingress
in New Jersey, USA
Joanna Burger
Division of Life Sciences, Rutgers University, 604 Allison Road, Piscataway, New Jersey 08854 USA
Abstract.—The management of threatened and endangered species often falls to various state agencies which
may have different and conflicting goals. The Pine Barrens of New Jersey are managed for different objectives,
including fire management, tree cutting, recreational activities (hiking, hunting, off-road-vehicle use), wildlife
protection, and conservation. Managing competing claims requires ecological information on critical issues and
vulnerabilities for determining the impacts of each claim. The Northern Pine Snake (Pituophis melanoleucus),
an iconic Pine Barrens species that is threatened in New Jersey, is normally dispersed during spring and
summer, but the snakes converge in the fall to communal hibernacula, where they spend the winter and leave
in the spring. Here, the activity of Northern Pine Snakes near hibernacula in the fall is described to examine
their vulnerability to various competing claims, such as fire or off-road vehicle use. Two hypotheses are tested:
(i) that snakes enter the hibernaculum once (and stay), and (ii) that the total period of ingress for all Northern
Pine Snakes is limited to just a few weeks in the fall. Activity of PIT-tagged snakes at hibernacula entrances
was monitored with a passive, continuously-recording AVID TracKer and temperatures were monitored with a
continuously recording thermometer placed at the soil surface. The behavior of marked snakes (18 in 2017, 25
in 2018), indicated that the period of activity around the hibernaculum entrance was: 1) longer than expected
(i.e., over two months), 2) involved multiple ingress and egress of individual snakes, and 3) sometimes involved
movement between two or among multiple nearby hibernacula. Northern Pine Snakes generally did not move in
or out of hibernacula when temperatures were below 9° C. Daytime high and nighttime low temperatures greatly
influenced movement. Although the daily high and low temperatures when snakes moved were correlated (r=
0.54 in 2017; 0.51 in 2018, P< 0.0001), the daily high and low temperatures were more highly correlated (r= 0.71
in 2017; 0.79 in 2018), indicating factors other than temperature influence snake activities. Most snakes entered
and exited between 1000 and 1800 h, although some moved as late as 0030 h. These data can inform science-
based decisions about when to allow tree cutting, fire management, and off-road vehicle races (e.g., increased
human activity). Most snakes are concentrated around hibernacula (but not necessarily near the entrances)
from early October until early December (or the end of December for two hatchlings). Therefore, a significant
proportion of snakes are vulnerable to disturbances that could impact their population viability. Vulnerabilities
are discussed in terms of competing claims and conservation.
Keywords. Behavior, competing claims, hibernation, reptiles, Serpentes, Squamata, wildlife management
Citation: Burger J. 2019. Vulnerability of Northern Pine Snakes (Pituophis melanoleucus Daudin, 1803) during fall den ingress in New Jersey, USA.
Amphibian & Reptile Conservation 13(2) [General Section]: 102-114 (e191).
Copyright: © 2019 Burger. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 In-
ternational (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows:
official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 14 January 2019; Accepted: 22 September 2019; Published: 6 November 2019
Introduction
Managers are often required to make environmental re-
source decisions with incomplete knowledge, with little
time, and often under conditions of competing claims for
resources and associated habitat. Human alteration of
natural lands is a key driver of global biodiversity loss
(Pimm and Raven 2000; Wilcove et al. 2000). Claims
for land can come from those who want to either use the
Correspondence. burger@dls.rutgers.edu
Amphib. Reptile Conserv.
resource itself (e.g., hunting, fishing, wildlife collect-
ing), use important components of the habitat (e.g., log-
ging), or improve the habitat for people (e.g., trail or road
building, fire suppression). Indeed, managers of differ-
ent resources (e.g., timber, wildlife) are often in conflict,
asserting competing claims for the same resource or hab-
itat. These need to be carefully considered and resolved
in a manner that reduces the risks to the habitat and
wildlife, while enhancing human benefits. For example,
November 2019 | Volume 13 | Number 2 | e191
Burger
managers of forests must balance cutting (or harvesting)
trees against re-forestation, the adverse effects of cutting
trees against the benefits of cutting them, and the relative
importance of the different benefits and costs (McLeod
and Gates 1998; Todd and Andrews 2008). Similarly, fire
suppression has some benefits (e.g., reduced potential for
fire damage to nearby communities and industries), as
well as costs if it does not occur (e.g., allowing dry debris
to build-up, creating the potential for a very hot canopy
fire when it does occur). Each option (e.g., logging, fire
suppression) has both benefits and costs to the plants and
animals living in the forests (Roth and Franklin 2018;
Steen et al. 2010). In addition, most animals face one or
more challenges to their survival, including predators,
competitors, poachers, and resource users, as well as
threats to their habitat from development, wildfire, or re-
source use. What may be good for one animal group may
not be good for another. For example, creating gaps in
forests may be good for deer management and for snakes
requiring open nesting areas, but is not good for interior-
nesting forest birds (Blouin-Demers and Weatherhead
2001; Gerald et al. 2006; MWPARC 2009). The complex
situations forest managers face can only be resolved by
examining the ecological and societal benefits and costs
of different options.
Setting priorities for conservation is a challenging
and necessary effort (Pimm et al. 2001). The biodiver-
sity crisis facing the Earth suggests that the conservation
needs of threatened and endangered species should be
considered first when managing habitats and ecosystems
(Wilson et al. 2009; Gaiarsa et al. 2015). Economic, soci-
etal, and political issues also play important roles in con-
servation decisions (Polasky 2008; Wilson et al. 2011).
However, it is equally important to understand the roles
of species vulnerability (UCN 2009), habitat loss (Wil-
son 1992: Pimm et al. 1995: Gibbons et al. 2000), habitat
fragmentation and patch size (Forman and Godron 1986;
Hilton-Taylor 2000; Kjoss and Litvaitis 2001; Sander-
son et al. 2002), restricted range or habitats (Segura et
al. 2007; Cardillo et al. 2008), human disturbances (Par-
ent and Weatherhead 2000), human infrastructures (e.g.,
roads, Andrews et al. 2008), and environmental stochas-
ticity (Tanentzap et al. 2012), among others (Gaiarsa et
al. 2015). Non-random distributions in time and space are
important aspects of vulnerability for animals, particular-
ly those that are slow moving or temperature-dependent
(Croak et al. 2013), including ectothermic vertebrates
(Kapfer et al. 2010). Understanding temporal and spatial
use of core areas 1s critical for conservation and manage-
ment (Semlitsch and Bodie 2003). All of these factors be-
come more important for understanding life histories and
conservation when they are considered within a frame-
work of human-related activities and impacts (e.g., fire
management, logging, development; Kapfer et al. 2010).
One of the iconic species of the New Jersey Pine Bar-
rens is the Northern Pine Snake (Pituophis melanoleucus
Daudin, 1803), a top-level predator that can reach 2 m in
Amphib. Reptile Conserv.
length. The Northern Pine Snake is listed as a threatened
species in New Jersey and as threatened or endangered
in other parts of its range in the southern United States
(Burger et al. 2017, 2018). New Jersey appears to have
the most stable population of this species (thus, a more
global responsibility for its conservation, Golden et al.
2009; Burger and Zappalorti 2016; Burger et al. 2017).
This paper examines the behavior of individually PIT-
tagged Northern Pine Snakes during their fall ingress
into hibernation sites (hibernacula or winter dens) in re-
lation to conservation of the species with respect to forest
management (e.g., logging, fire suppression) and other
human activities (e.g., poaching, off-road vehicle [ORV]
races, and traffic). There are competing claims for the
habitat (e.g., snake use and ORV use), for habitat man-
agement (e.g., fire management and deer management),
and for the snakes themselves (e.g., population stability
and poaching, Burger and Zappalorti 2016). The activi-
ties of snakes in the fall were monitored around several
hibernacula using new passive PIT-tag recording devices
located at the hibernaculum entrances. This technical ap-
plication is described with the intent of illustrating its use
for other such studies. The overall goal was to test the
null hypothesis (H,) that Northern Pine Snakes return to
their hibernacula and enter only once, remaining there
for the duration of the winter hibernation period. If H,
is rejected, this could indicate increased vulnerability in
time and space for a snake that is already threatened in
New Jersey.
Hibernation behavior in this species has been studied
previously in terms of hibernaculum site selection, use
and fidelity, structure of hibernacula, and the defensive
behavior of snakes disturbed during hibernation (Burger
et al. 1988, 2000; Burger and Zappalorti 2016, 2017).
Hibernaculum sites of other species of pine snakes (P.
ruthveni and P. melanoleucus lodingi) were studied in
Mississippi where the former used burrows of small
mammals, and the latter used decayed pine stumps and
roots for hibernation (Rudolph et al. 2007). Dispersal
rates around hibernation sites were also examined in
Gopher Snakes (Pituophis catenifer deserticola) in Brit-
ish Columbia (Williams et al. 2012). Some studies on
hibernation in other snake species include hibernation
site selection (Harvey and Weatherhead 2006), body
temperatures while hibernating (Costanzo 1986; Hein
and Guyer 2009), cold tolerance (Joy and Crews 1987),
factors affecting spring emergence (Todd et al. 2009),
spring emergence patterns (Hirth et al. 1969; Gregory
1974; Shine et al. 2006), and gene flow among snakes in
different hibernacula (Clark et al. 2008; Anderson 2010).
However, without individually marked snakes, and the
availability of the recent remote recording ability of the
Avid Power TracKer VIII, it was previously impossible
to determine the activity of individual snakes near hiber-
nation sites, the final entry temperatures for fall ingress,
or the final dates of entry into hibernacula, each of which
were incorporated into the present study.
November 2019 | Volume 13 | Number 2 | e191
Pituophis melanoleucus vulnerability during fall ingress
Temp
Reader
Den Entrance
PiTTag
Snake Cement Reader
Den Block (buried
Tunnel under soil)
Ss ya Data
Logger
Battery
12 Volts
Fig. 1. Schematic of deployment of the Tracker device at the entrance of a hibernaculum.
Methods
Northern Pine Snakes have been studied in the Pine Bar-
rens of New Jersey for over 35 years, including marking
each snake with an individual PIT tag (Burger and Zap-
palorti 2011). They are large constrictors that reach the
northern limit of their range in southern New Jersey. The
New Jersey population is separated from other popula-
tions by several hundred km (Golden et al. 2009; Burger
and Zappalorti 2011, 2016). They dig their own nest bur-
rows, and dig or modify hibernacula (Burger and Zappal-
orti 2011). They hibernate communally, along with other
snake species.
Northern Pine Snake studies have examined breed-
ing and hibernation biology, risks and threats Northern
Pine Snakes face, habitat selection, movement and home
ranges, and contaminant exposure. While movement has
been studied throughout the year with the use of radio-
tracking, these previous studies did not provide detailed
movement of the community of snakes using hibernacula
(Burger and Zappalorti 2011). During this period North-
ern Pine Snakes were studied in Burlington, Cumber-
land, and Ocean counties, however, the exact locations
of the studies were not disclosed because of the very high
risk of poaching of Northern Pine Snakes (Burger et al.
2017, 2018).
The present study used passive continuous recording
devices on snakes as they left and entered the hibernac-
ula. In 2017 one hibernaculum was monitored to test the
feasibility of using this tracking method, and in 2018, five
hibernacula were monitored (four units monitored snakes
for the entire year in Bass River State Forest, and one
additional site was only monitored in the fall in Berkeley
Township, Ocean County, known as “Davenport Den’).
Any tagged snake passing by, entering, or leaving one
of these monitored hibernacula was recorded. Data were
generally down-loaded every 2—3 weeks throughout the
Amphib. Reptile Conserv.
year. A recording device was placed at the entrance of
each hibernaculum, and buried so it was not visible (Fig.
1). The device used was the AVID Power TracKer VIII,
a multi-mode reader with memory for PIT tags, made by
AVID Identification Systems, Inc., in Norco, California.
A TracKer unit was placed at each hibernaculum entrance
and covered with a | cm layer of sand to prevent vandal-
ism. The unit has a 6-inch coil reader with leads that can
be up to 4 m long and lead to a device that can record and
store up to 2,500 events, recording the PIT Tag, the time
of day, and the date for each event. The power source was
a 12-volt marine battery. The recorder and battery were
placed in a plastic box, covered with a board for stability
(and to prevent collapse if someone stepped on it by ac-
cident), buried beneath 10 cm of soil, and covered with
leaves and twigs for camouflage (Fig. 1). None of the
equipment was visible on the surface to prevent injury of
the snakes, theft, or vandalism. The technology requires
that snakes are fitted with PIT tags. Although the record-
ers were operating all year, this report only examines
snake activity from 15 October to 31 December 2017 (at
one hibernaculum) and from 1 October to 31 December
2018 (at five hibernacula).
The soil surface temperatures were recorded continu-
ously, all year, near one of the hibernaculum entrances at
Bass River State Forest using an Elitech RC-SUSB Tem-
perature Data Logger. The device was placed in a plastic
bag and covered with a 1 cm layer of sand and moss to
disguise its location. In previous studies, this small re-
corder has worked for well over a year on its original
battery.
This study was only possible because: 1) Many North-
ern Pine Snakes use the same traditional hibernation and
nesting sites (Burger and Zappalorti 2011; Burger et al.
2012; Zappalorti et al. 2014), 2) Gravid female Northern
Pine Snake use the same hibernating and nesting sites
(Burger and Zappalorti 1992, 2015), 3) Hatchlings can
November 2019 | Volume 13 | Number 2 | e191
Burger
2017
All activity
Den 1
Temperature °C
“Oi, “OO, Oe
Date
Temperature °C
Reader Down
012007546
841005587
020795281
840890092
012261123
020585572
021079007
021285039
0213009019
021381340
021836516
014534620
021542803
021608772
021631878
841019086
014534324
020891883
Fig. 2. All activity of snakes at den 1 (Bass River State Forest) in 2017 as a function of date and soil surface temperature. The
colored markers indicated by 9-digit numbers in the legend represent individually tagged snakes. Data for snakes during the period
from 29 October to 11 November (red line) were not recorded because the maximum number of data points the receiver could store
was reached.
be easily found at nesting areas, fitted with PIT tags, and
then followed at the hibernacula, and 4) Therefore, most
of the individual snakes using a given hibernation site are
PIT-tagged. Further, the sexes and ages of all snakes were
known because they had been followed since they were
hatchlings or two-to-three years old. The hibernacula in
this study had been studied for over 30 years, and were
well-known to the snakes and the researchers (Burger
and Zappalorti 2011; Burger et al. 2012). For each snake,
the first reading hit of the season was assumed to be its
initial entry.
Analyses included calculating frequencies, percent-
ages, means, and standard deviations for various be-
havior parameters of the Northern Pine Snake around
hibernation sites in the fall. Data were analyzed using
standard SAS software (Statistical Analysis Systems,
Cary, North Carolina, USA), including Kruskal-Wallis
One-Way Analysis of Variance (ANOVA), with 95%
confidence intervals. Kendall tau was used to determine
correlations among ambient soil surface temperatures
and the temperatures at which snakes exhibited activity.
The best models for explaining variations in snake activ-
ity as a function of temperature and date were developed
using SAS (ProcGLM) procedures. Variables included
were den, year, age, sex, date (only for the temperature
model), and maximum and minimum daily sand surface
temperatures.
Amphib. Reptile Conserv.
Results
Date and temperature: The two primary factors that
might account for entry of Northern Pine Snakes into hi-
bernacula in the fall are date and ambient temperature.
The factors entering the best model (F = 34, P < 0.0001,
r’ = 76) for Julian date of activity (e.g., entering/leaving)
were maximum daytime sand temperature (P < 0.001),
den number (P < 0.04), and perhaps age (P < 0.08). The
factors entering the best model (F' = 122, P < 0.0001, r?
= 90) explaining variation in the temperature of snake
activity (1.e., soil surface temperature when a snake en-
tered, left, or passed by the hibernaculum) were maxi-
mum daytime sand temperature (P < 0.001), minimum
nighttime temperature (P < 0.0001), and sex (P < 0.04).
These factors are explored in greater detail below.
Seasonal activity patterns: While there was virtually
no activity around the hibernacula in August or Sep-
tember, by early October snakes returned to the vicinity
of the dens and began passing by, entering, and leaving
hibernacula. In 2017, the equipment was only deployed
in mid-October (when activity was expected to begin) at
Bass River State Forest, but many snakes were already
active around den | (Fig. 2). In the first year the reader
was initially placed 0.3 m down the tunnel to the hiber-
naculum, and this resulted in one snake sitting in the en-
trance, and running the recorder until it reached the max-
105 November 2019 | Volume 13 | Number 2 | e191
Pituophis melanoleucus vulnerability during fall ingress
Temperature °C
Temp
021804062
845090777
012261123
012077546
021608772
841017858
20795281
841004858
021626044
013091070
014534620
011564817
021080090
021542803
021791327
841007010
014534324
021280836
014843117
= 5 i} | | I }
FEA
“Q. “B. ‘0. ‘o “By. “ y “D. “y. “D. “y. her Le 47, CL aa oh tin oh, td, CL for 014263843
fy. % a f; 4, iG So Ry Yo O- g “> v4 fp 8s? — ? . ce
i, <7) : A) ») “3 by 2, pce we &) E> ty Sy 7) Qy “3 Je S. ») 4 > “ a) 25 7) 845090803
~ ~ ~~ ~ ~ “f/f + ~ ~ ~ ~ ka “4 “fy ~ ~ ool C mel
“p tp “ip “Oz. “Oz, ~Op, “Op, “Or, “Or, “Op, “Gp, “tp “dp “Up “Oz, “Op, “Oy, “Op, “Oz, “Op, “Op, “tp
Date
021285039
021381340
836521818
845091087
Fig. 3. All activity of snakes at four dens in Bass River State Forest in 2018 as a function of date and soil surface temperature.
imum number of data points it could store (n = 2,500).
Figure 2 also indicates the period when the recorder was
not recording. Because of this, the recorder was moved
up to the entrance on 9 November 2017 (so that even if a
snake was in the tunnel, watching the outside world with
its head at the entrance, it would not record the activity
more than a few times). During this down period from 29
October to 9 November some snakes entered (and may
have left) without being recorded. Even so, the pattern
clearly shows 18 different snakes (ages 0 [hatchling]
to 16 years) entering, leaving, and re-entering from 16
October to 17 November 2017. The recorder continued
monitoring through December but due to freezing sur-
face temperatures, there was no more activity.
In 2018, the activity of 25 Northern Pine Snakes be-
gan on 2 October and continued to 7 December at Bass
River State Forest (Fig. 3). The pattern was similar to that
in 2017 in that there was daily temperature variation, and
the snakes entered and left numerous times. It is, how-
ever, important to acknowledge these patterns because
they show that activity is rather constant. Thus, the first
hypothesis of a restricted time period of activity around
the hibernacula was rejected.
Additionally, the Davenport Den (Ocean County) was
monitored in the Fall of 2018. In winter of 2017-2018
only one two-year old Northern Pine Snake and two Corn
Snakes Elaphe guttata (now Pantherophis guttatus) used
this hibernaculum. In the fall of 2018, it was used by two
hatchlings and the same two-year old. There were thus
Amphib. Reptile Conserv.
106
no large snakes that might influence the activity of the
small Northern Pine Snakes; and the hatchlings were ex-
tremely active. The activity at this hibernaculum started
on 1 November and ended on 28 December 2018. Since
there were so few snakes at this hibernaculum, the in-
dividual activity patterns of the hatchlings are given in
greater detail below.
Time of Day: As might be expected for ectothermic spe-
cies, snakes were most active during the day and more
so on warm sunny days. Most activity occurred between
1000 and 1700 h in both years (Fig. 4). In 2017, 77% of
the activity occurred between 1000 and 1600 h; in 2018,
84% of the activity occurred in this same time period.
However, in 2017 one snake left at 2000 h, and in 2018,
one entered at 2045 h, and another entered at 0100 h at
night. These rarely observed nocturnal activities occurred
during relatively high temperatures (> 14° C).
Temperature effects: The activity of the snakes was
plotted against the soil surface temperatures for 2017 and
2018 as a function of date (Figs. 2 and 3). In both years,
the October surface temperatures were high, and they
generally decreased throughout the fall. Snakes did not
enter or leave at the lowest daily temperature (at night),
but sometimes entered or left at the highest temperatures
for the day. Most of the activity occurred at temperatures
of 10° C or above. In both years there was little activity
when the surface temperature fell below 8° C at night.
November 2019 | Volume 13 | Number 2 | e191
Burger
Bass River State Forest
Fall 2017 (1 den)
aa 4
a
é aé
7 o* tye ma 1
eo e
a
reg é A e
10 @ Final Winter Entry
e@ Entering
4 Leaving
/ Z / f
a7) “Op *ay °0 ®a “Og “Op
@ Final Winter Entry
Surface Soil Temperature (Celsius)
Pr e Entering
e
25 me ~" 5% aos 4 Leaving
a ¢
20 a « Passed Entrance
e 4 @a
15, @ as é a ~ f
‘4 ren Ke 7
a P| ny aan
10 .45 a
= 8
5 r=0.1
Ga, Ba, “Oy 2a, “Lo, ‘6, op 18. Op <0. Qn <2. Op Vy,
Time of Day
Fig. 4. Fall activity of snakes in Fall 2017 and Fall 2018 as a
function of time of day and surface soil temperature. Activity
type 1s noted by each symbol.
However, it is noteworthy that for both years, snakes en-
tered or left the hibernacula, even after prolonged periods
of daily low temperatures that reached 0° C in 2017, and
even -5° C in 2018 (Figs. 2 and 3).
Although the daily high and low temperatures and
snake movements were correlated (7 = 0.54 in 2017; 0.51
in 2018; both P < 0.0001), the daily high and low tempera-
tures for each day were more highly correlated (r = 0.71
in 2017; 0.79 in 2018, Fig. 5). Figure 5 indicates when
snakes either entered or left a hibernaculum, or made their
final entry for the winter. Note that some snakes entered at
the same temperature point, and so there are fewer points
than snakes. There are fewer points in 2017 because only
one hibernaculum was monitored; while the 2018 data re-
fer to all four hibernacula at Bass River State Forest. Final
entries were usually at lower temperatures than other ac-
tivities (Fig. 5).
Individual behavior: Figures 2—3 indicate frequent ac-
tivity at hibernacula; individual snakes typically entered
and left more than once (rejecting the initial hypothesis).
The activity of individual snakes was examined only for
2018; individual activity in 2017 was not examined be-
cause equipment failure for a short period made it impos-
sible to know whether any snakes left or entered during
that period. Some snakes entered a den and remained for
the winter (32%), but most did not (68%). At the Bass
River study site, some snakes visited all four of the moni-
tored hibernacula on the same day, often returning to the
first one they entered. Snakes entered or left hibernacula
Amphib. Reptile Conserv.
Out
Final
Entry
Previous Night Low Temperature (Celsius)
Early Sept
ma
7%
ry
e
a
e
Ne 4 a -
Out
xe)
Final
Entry
Previous Night Low Temperature (Celsius)
Pass
“10 15 20 25 30 35
Max Daytime Temperature (Celsius)
Fig. 5. Activity of snakes in Fall 2017 and Fall 2018 as a func-
tion of the maximum daytime temperature and the previous
night’s low temperature.
an average of 5.6 + 0.7 times, switched dens an average
of 1.4 + 0.3 times, and visited 1.8 + 0.2 dens at Bass
River State Forest in 2018. Movement was a function of
age: older snakes moved more often than younger ones
(Table 1). At Bass River State Forest, hatchlings moved
an average of only 2.3 + 1.3 times (Table 1).
However, at the Davenport den, where there were only
two hatchlings and one 2-year old, the movement pattern
was very different. Hatchlings used the hibernaculum as
a home base, and went in and out many times before final
entry. Sometimes they remained near the entrance, but
they mainly moved a few meters away (e.g., the hatch-
lings were not immediately located). The seasonal pat-
terns of the two hatchlings are shown in Fig. 6. The two
hatchlings moved 48 and 66 times, while the 2-year old
moved only 16 times. The lack of older, larger Northern
Pine Snakes at the den may have allowed the hatchlings
to move more freely.
Activity around each den (entering, leaving) varied
significantly (X? = 98, P < 0.0001), and the percentage of
hits at each den varied: den 1 = 25%, den 2 = 59%, den 4
= 12% and den 5 = 4% of total activity at Bass River. The
total activity around the four dens at Bass River State
Forest was 139 hits for 25 snakes. At the Davenport den
November 2019 | Volume 13 | Number 2 | e191
Pituophis melanoleucus vulnerability during fall ingress
Table 1. Movement of Northern Pine Snakes among four monitored hibernacula at Bass River State Forest, New Jersey, USA, in 2018.
Age of Snake (yr)
0-1 2-3 5-7 Over 7 ».G
Any Reading
mean 2.3 1.3 2.8+0.9 6.8+2.5 7140.8 8.7 (0.03)
min/max 1/6 1/5 1/11 Srl
Den Switches
mean 0.3403 0.5+0.5 135207 2.0+0.4 8.0 (0.05)
min/max 0/1 0/2 0/3 0/5
Dens Visited
mean 1.3403 1.3+40.3 1840.3 220.2 7.9 (0.05)
min/max 1/2 1/2 1/2 1/4
845*090* 639 ——— Temperature C
—*e— Snake Activity
Temperature °C
845*090*603
Temperature °C
a Lae “Le. Ly, Pg 2s LR; 1) Ones Ons Ss
24 gy, 2b, 20, 04,07 “07, gb, 20, °0, 0, yO
PILE OP PR FE Ly PN a EEE GE Me tee
Date
Fig. 6. Activity of two hatchlings (tag numbers 845090639 and 845090603) in the fall of 2018 at den (Davenport) as a function of
date and soil surface temperature.
Amphib. Reptile Conserv. 108 November 2019 | Volume 13 | Number 2 | e191
Burger
HIBERNATE
(leave in April)
Rest, Bask Forage Reproduction
Seek Mate
Mate
ge ci bees
oe Female
Dig Nest
¢o coe? Lay Eggs
60 days |
Eggs Hatch
Forage
Hatchlings
Emerge
Enter Hibernacula
(Oct-Dec)
Fig. 7. Schematic of life cycle of Northern Pine Snakes, in-
dicating periods of high vulnerability to human disturbances,
such as fire, off-road vehicles, hunting, and poaching.
it was 120 hits for only three snakes, and the two hatch-
lings accounted for most of this activity.
Discussion
Methodological issues and using the Power TracKer
VIII: Any study of animals in the wild is fraught with
variability and uncertainties in the methods used, in en-
vironmental variation, and in the behavior and ecology
of the species. Data from 2017 indicated that the PIT-tag
recording devices could be used in the field with 12-volt
marine batteries, since they operated properly, and the
data could be retrieved. However, the main problem en-
countered initially related to placement of the receiver
— when it was partway down the hibernaculum entrance,
it recorded continuously as some snakes simply rested in
the tunnel, peering out of the entrance and filling all the
available data points. When the coil was moved to the
front of the entrance, this problem did not exist, but then
it was difficult to determine if a snake merely passed by
the entrance, or entered. This issue could be partly man-
aged by seeing where the individually marked Northern
Pine Snake turned up next. The main difficulty with the
Power TracKer was that the batteries need to be changed
to allow charging every 2—3 weeks depending upon tem-
perature (battery life was shorter at cold temperatures).
Batteries need to be charged on the “slow setting” rather
than the “rapid method;” as the former provided a longer-
lasting charge in the field. Bad weather, heavy rains and
snow, and downed trees from severe storms made getting
to the study site to change the (20 kg!) batteries every
couple of weeks very challenging.
Poaching of Northern Pine Snakes is known to be a
major threat (Burger and Zappalorti 2016), so I opted not
Amphib. Reptile Conserv.
to use solar power or place cameras that might call atten-
tion to the den entrance. Visible solar panels would alert
poachers or vandals to the exact location of hibernacula
entrances, and would also encourage theft. Protecting
the equipment is important since each set-up costs about
$3,000 for the TracKer, leads, batteries, plastic case for
the recorder and batteries, and a wood cover to prevent
excessive rain from entering the plastic case. The con-
tinuously recording thermometers were only $25, and
the manufacturer’s battery lasted at least a year. Lastly,
the tracker should be put in place when the snakes are
underground to ensure that they leave a scent trail when
they leave so that other snakes (particularly hatchlings)
can find the entrance.
With any field study there are weather-related and
other environmental variables that can influence the
behavior of the snakes. Exceptionally warm weather in
2018 resulted in an extended period of ingress into the
hibernacula. No snake entered or left den 1 in 2017 (the
only den monitored that year) after 17 November, but in
2018 snakes continued to move in and out of the five
dens monitored into late December.
Finally, there are uncertainties that relate to the behav-
ior and ecology of the snakes. These uncertainties were
related to age, sex, and individual responses. Age clearly
entered as a factor in explaining the observed Northern
Pine Snake behavior, but this would not have been clear
if the snakes were not of known ages. The behavior of
hatchlings varied depending upon the composition of
the hibernaculum community (see below). Hatchlings
moved very little when they were part of a community
that included snakes of different ages (and sizes), but
hatchlings moved often when there were no larger (older)
snakes present.
Activity patterns around hibernacula in the fall:
Northern Pine Snakes in the present study were very ac-
tive around the hibernacula for over two months. At Bass
River State Forest, snakes moved in and out an average
of six times, often switching dens. The hypotheses that
activity around a hibernaculum was restricted in time,
and that snakes entered a hibernaculum and stayed were
both rejected. Individuals moved from den to den over a
few days or a few weeks, partly dependent upon weather.
That Northern Pine Snakes left a given den and did not
enter another den for several days, but then returned, in-
dicates that there are some other suitable places to shelter
when the temperatures drop at night. Nonetheless, the
snakes came back to one of their original dens when the
weather warmed up enough to move.
The factors that played a role in activity were sea-
son (date), temperature (daytime high and nighttime
low), age, and hibernaculum number. The Northern Pine
Snakes appeared to prefer two of the dens over the oth-
ers. However, even snakes that first entered one of the
“preferred dens” moved to other dens before returning.
One might predict that older snakes, aware of the advan-
tages and disadvantages of one den over another, might
November 2019 | Volume 13 | Number 2 | e191
Pituophis melanoleucus vulnerability during fall ingress
move less than young snakes that are less familiar with
their environment and den options. This, however, was
not the case. The reason for increased switching with in-
creasing age 1s unclear. However, in the absence of larger
(older) snakes, the two hatchlings at the Davenport den
(an isolated hibernaculum) used it as a home base, and
moved in and out frequently, depending upon tempera-
ture. These two hatchlings did not finally enter for the
winter until 28 December.
Factors affecting entry into hibernacula: Clearly
there are seasonal and temperature effects; Northern
Pine Snakes enter hibernacula to avoid freezing winter
temperatures, as do other snakes in northern climates.
Although other studies have examined the temperatures
of snakes during hibernation (Costanzo 1986; Hein and
Guyer 2009), or emergence in the spring (Todd et al.
2009), little is known about the temperatures at which
snakes enter hibernacula in the fall. To study fall behav-
ior requires: 1) individually marked snakes, 2) a method
of recording each snake’s entrance in the fall (date, time
of day), and 3) devices to continuously record the soil
surface temperature to capture the temperature when
snakes enter. A long-term study was required for the first
criterion, and recent technological developments were
required for the latter two. The development of this new
technology makes it possible to more accurately examine
both the seasonal and temperature influences on snakes
entering and emerging from hibernacula, as well as indi-
cating the degree to which snakes move in and out dur-
ing both entry and emergence, before finally dispersing
in the spring to forage, mate, and nest.
In this study, date and sand surface temperature de-
termined when snakes entered and left hibernacula, and
snakes moved an average of about six times before set-
tling in for the winter. Three other factors seemed to also
affect movement: den number, age of the snakes, and for
hatchlings, the presence of older (larger) snakes. Snakes
clearly preferred two of the monitored dens over the oth-
er two, and both of the preferred dens were deeper than
the other two, and they were older in terms of usage his-
tory (Burger and Zappalorti 2011).
The age of the snakes influenced their movement;
older snakes moved more often, switched dens more
often, and visited more dens than did younger snakes.
This was unexpected since younger snakes might be ex-
pected to explore a range of different sites before settling
down. Hatchlings using the four hibernacula at the Bass
River State Forest showed significantly less activity than
older snakes (an average of only two movements/snake).
However, the two hatchlings that used the Davenport hi-
bernaculum showed activity 48 and 66 times. They not
only entered and left (and were not visible around the
hibernaculum or in the surrounding area), but sometimes
basked very near the entrance, moving swiftly down the
entrance when approached by the researchers. They ap-
peared to be using the hibernaculum as a refuge and an
Amphib. Reptile Conserv.
overnight site for nearly two months before remaining for
the winter (refer to Fig. 6). This difference in hatchling
behavior at the two sites may relate to the relative risk
posed by much larger snakes using the same hibernacu-
lum. If large, heavy (up to 1,350 g) adult snakes are en-
tering and leaving, they pose a risk to hatchlings (30—50
g), and adults could injure them while both are moving
through the tunnels. The only dead snakes found tn hiber-
nacula over the years (with one exception of small mam-
mal predation) were those squashed flat by older, larger
snakes lying on top of them for long periods of time.
Vulnerability, risk, and competing claims: Northern
Pine Snakes are most vulnerable when they are roaming
above ground (even though they are partially fossorial),
and when they are concentrated in one small area. They
are above ground at intermediate temperatures; 1n the hot
summer they spend a great deal of time in hollow fallen
logs, under leaves and needles, or underground; in the
winter they hibernate 1—2 m below ground. Behaviorally
they are vulnerable when they are mating (spatially scat-
tered), nesting (females, spatially clumped), and entering
or leaving hibernacula (clumped around hibernacula).
The vulnerability of Northern Pine Snakes is greatest
when these two features (above ground and clumped)
overlap, which occurs when entering hibernacula for the
winter. This situation occurs when entering hibernacula
for all Northern Pine Snakes, and for females when they
are nesting (Burger and Zappalorti 1992, 2011, 2016;
Burger et al. 2017, 2018, Fig. 7). The data presented in
this paper clearly show that the period of ingress into hi-
bernacula is at least two months in duration, spanning
both October and November, and can extend through
December if the weather is not too cold. The data also
show that there is frequent activity, not just one entry into
the hibernaculum by each snake. The dens at Bass River
State Forest that were studied are about 30-120 m from
each other. That snakes come and go indicates that the
spatial area of activity is greater than just around the 1m-
mediate entrance to a hibernaculum.
Only once was a Northern Pine Snake seen above
ground in the fall, although later analysis of the recorded
data indicated that just minutes before or after our pres-
ence, snakes entered or left the hibernaculum. In one
case, a snake came up five minutes after we finished
downloading the data, and I only saw it because I went
back to pick up a piece of equipment. It was lying in the
tunnel, with its head about 2 cm from the entrance. This
observation emphasizes the importance of having con-
tinuously recording equipment; observation alone would
not yield this key information.
The major risks that Northern Pine Snakes face are
natural predators (hawks, mammals, and other ophi-
ophagus snake species), commensal predators (dogs,
raccoons), poachers, loss of habitat, and human distur-
bance (direct and indirect). Human disturbance can take
the form of people disrupting snake behavior (e.g., dur-
November 2019 | Volume 13 | Number 2 | e191
Burger
ing snake copulation, nesting, or entering/leaving hiber-
nacula), disrupting snake habitat (e.g., off-road vehicles,
ORV races through the Pine Barrens, prescribed burns,
tree-cutting), or a combination of these activities. Many
of these activities represent competing claims for the
same Pine Barrens habitat (either quantity or quality of
the habitat).
The resolution of competing claims for Pine Barrens
habitat, or management of that habitat, 1s partly a societal
decision. However, the specific needs of wildlife, and of
specific species such as the Northern Pine Snake, cannot
be considered unless there are data to show what those
needs are, when (and what) their vulnerabilities are, and
when interference will jeopardize their populations. In
many cases, a situation can be resolved by bringing to-
gether the relevant people and agencies, and determining
the best course of action. Clearly, debris and dry leaves
that will result in a hot fire that could destroy local hu-
man communities or businesses (as well as wildlife) need
to be reduced, and fire management is a reasonable op-
tion. Likewise, hunting, ORV races, and other human ac-
tivities are reasonable uses of public forests such as the
Pine Barrens. Protection of endangered and threatened
species is another public goal (as well as being a legal
one) that must be considered. Even accepting the latter
as an important public goal does not completely solve the
problem, however, because different species may have
different requirements and vulnerable periods. For each
species, relative abundance and total distribution need to
be considered, with species which have very restricted
ranges getting priority treatment. A consensus needs to
be reached both about the specific habitat and ecologi-
cal requirements of different endangered, threatened, or
otherwise vulnerable species, and about the specific re-
quirements of other groups with competing claims (e.g.,
foresters, recreationists, fire managers). Armed with this
knowledge, managers can make science-based, societal-
ly-based, and cost-effective decisions about managing
the habitat and the associated wildlife species that occur
there.
Conclusions
Plants and animals in the Pine Barrens, and everywhere
else, face competing claims to their habitat along with
of the risks of disruption or disturbances from other ani-
mals, poachers, recreationists, foresters, resource manag-
ers, firemen, developers, and the general public. Resolv-
ing competing claims requires having knowledge of the
specific needs of vulnerable species and habitats, as well
as the needs of the people and managers. One high risk
vulnerable period for Northern Pine Snakes is when they
enter or leave their winter hibernation sites. This paper
provides data showing that the fall ingress period to hi-
bernacula is prolonged (over two months), and involves
frequent snake activity above ground. During October
and November in the Pine Barrens, Northern Pine Snakes
Amphib. Reptile Conserv.
are moving toward hibernacula, concentrating there, and
entering and leaving frequently until they eventually stay
underground for the winter. Thus, this is a highly vulner-
able period when snakes are concentrated, and any dis-
ruptions (such as fires or off-road vehicle races) have the
potential to injure or kill Northern Pine Snakes that are
threatened in New Jersey, and threatened or endangered
throughout most of their range. New Jersey has perhaps
the largest, and most stable population of Northern Pine
Snakes throughout the range of the species (Golden et al.
2009; Burger et al. 2016, 2017), therefore state wildlife
agencies have a special responsibility to ensure its con-
tinued survival.
Acknowledgments.—I especially thank R.T. Zappalorti
and M. Gochfeld who have been part of these Northern
Pine Snake studies since the beginning, and E. DeVito,
who quickly joined us. I thank the many agencies and in-
dividuals who have helped study and preserve Northern
Pine Snakes in the New Jersey Pine Barrens, especially
Kris Schantz, David Jenkins, and Dave Golden of the
Endangered and Nongame Species Program, and Cyn-
thia Coritz of the Division of Parks and Forestry of the
New Jersey Department of Environmental Protection,
New Jersey Conservation Foundation, and Nature Con-
servancy. Over the years many Rutgers University ecol-
ogy graduate students and personnel of Herpetological
Associates have assisted in these studies. I particularly
thank Christian Jeitner, Kelly Ng, Matt McCort, David
Schneider, Mike Torocco, Dave Burkett, Ryan Fitzger-
ald, and Taryn Pittfield. This research was performed
under Rutgers University Protocol number E6—017, and
appropriate state permits. Funding has included sup-
port from Rutgers University, Herpetological Associ-
ates, New Jersey Conservation Foundation, and the Tiko
Fund, and I gratefully thank the many volunteers who
have cheerfully helped us throughout the 30+ years of the
study, including the teenagers who grew up to continue
helping, bringing their own children.
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Pituophis melanoleucus vulnerability during fall ingress
Joanna Burger is a Distinguished Professor of Biology at Rutgers University, as well
as a member of the School of Public Health, Institute for Marine and Coastal Sciences,
the Biodiversity Center, and the Environmental and Occupational Health Sciences
Institute. Joanna received her B.S. in Biology from the State University of New York at
Albany, her M.S. in Zoology and Science Education from Cornell University, her Ph.D.
in Ecology and Behavioral Biology at the University of Minnesota in Minneapolis,
Minnesota, and an honorary Ph.D. from University of Alaska. She is an ecologist,
human ecologist, behavioral biologist, and ecotoxicologist who has worked with several
species, including Pine Snakes, lizards, turtles, and sea turtles, for over 40 years in
many parts of the world. Joanna’s primary research has focused on behavioral ecology,
ecotoxicology, risk assessment, and biomonitoring. Additional research involves public
perceptions and attitudes, inclusion of stakeholders in solving environmental problems,
and the efficacy of conducting stakeholder-driven and stakeholder-collaborative
research. She has been a member of the Endangered and Nongame Species Council
since the mid-1970s, and has served on several National Academy of Sciences boards
and committees. Joanna has published extensively in the peer-reviewed literature, and
has written or edited over 25 books, including The Northern Pine Snake: Its Life History,
Behavior, and Conservation with R.T. Zappalorti.
114 November 2019 | Volume 13 | Number 2 | e191
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 115-125 (e192).
Teptile-cons™
From incidental findings to systematic discovery:
locating and monitoring a new population of the
endangered Harlequin Toad
1*Andrés Jiménez-Monge, ‘”*Felipe Montoya-Greenheck, ‘Federico Bolafos,
and °*Gilbert Alvarado
'Faculty of Environmental Studies, York University, Toronto, CANADA *Escuela de Antropologia, Universidad de Costa Rica, San José, COSTA
RICA 3Observatorio del Desarrollo, Universidad de Costa Rica, San José, COSTA RICA *Escuela de Biologia, Universidad de Costa Rica, San
Pedro Montes de Oca, San José, COSTA RICA *Laboratorio de Patologia Comparada de Animais Selvagens, Universidade de SGo Paulo, Sdo
Paulo, BRAZIL °Laboratorio de Patologia Experimental y Comparativa (LAPECOM), Escuela de Biologia, Universidad de Costa Rica, San José,
COSTA RICA
Abstract.—The scientific and conservation communities recognize toads of genus Atelopus as among the
most vulnerable of all amphibian groups, with over 75% of the species assessed as “Critically Endangered” by
the International Union for the Conservation of Nature (IUCN) Red List. Atelopus varius, known as the Harlequin
Toad, has been thought to be extinct in Costa Rica since the mid-1990s. There have been four rediscovered
populations of the species since 2004. This report presents the fifth reappearance of A. varius, this time in the
Alexander Skutch Biological Corridor (ASBC) in the Pacific Slope foothills of La Amistad International Park,
Costa Rica, which represents a new location. Previously, the pattern of reappearance of this species has been
unclear. In this study, the discovery of a new population of A. varius allows us to evaluate the presence of Bd
infection and offer critical natural history remarks. In total, 25 different individuals were identified. All samples
analyzed for Bd diagnosis were negative. In contrast to other A. varius populations, this one was mostly found
high above the riverbed, often in the foliage, tree trunks, and bromeliads, from 1-6 m above the water both
during day and night. The absence of Bd infection in these Harlequin Toads, a highly susceptible species, in
an area identified as having a high probability of Bd occurrence, suggests that this behavior could have helped
this population survive by reducing infection risk. Moreover, the distribution of A. varius may have changed
in the last 50 years, by penetrating higher in the montane regions of the Talamanca mountains, a change in
distribution that might also help its survival of some environmental stressors. With the discovery of a new
locality for A. varius, this study offers an animal behavior argument to account for species recovery in general,
as well as a possible expansion of what has been accepted as the historical distribution of this species.
Keywords. Ate/opus varius, natural history, citizen science, endangered species, chytrid fungus, Alexander Skutch
Biological Corridor, Costa Rica
Resumen.—Los sapos del géenero Atelopus son reconocidos como uno de los grupos de anfibios mas
vulnerables, con mas del 75 por ciento de las especies de este géenero evaluadas como “En Peligro Critico”
por la Lista Roja de la Union Internacional para la Conservacion de la Naturaleza. Se pensaba que Atelopus
varius, conocido como la rana Arlequin, se habia extinguido en Costa Rica desde mediados de los anos
noventa. Después de 2004 ha habido cuatro redescubrimientos de la especie. Este informe presenta la quinta
reaparicion de A. varius, esta vez en el Corredor Biologico Alexander Skutch (ASBC) en las estribaciones de la
vertiente del Pacifico del Parque Internacional La Amistad, Costa Rica como una nueva ubicacion. Hasta ahora,
el patron de reaparicion de esta especie no ha sido claro. En este estudio, con el descubrimiento de una nueva
poblacion de A. varius, ofrecemos importantes observaciones de historia natural y evaluamos la presencia
de la infeccion por Bd. En total, se identificaron 25 individuos diferentes. Todas las muestras analizadas para
el diagnostico de Bd fueron negativas. En contraste con otras poblaciones de A. varius, en nuestro caso se
encontro la mayoria de los individuos alto sobre el lecho del rio, a menudo en el follaje, troncos de arboles y
bromelias, entre 1-6 m sobre el agua, tanto de dia como de noche. La ausencia de infeccion por Bd en estas
ranas arlequin, una especie altamente susceptible, en un area identificada como con una alta probabilidad de
ocurrencia de Bd, sugiere que los sapos que pasen menos tiempo cerca del rio y mas tiempo en areas abiertas,
podria haber ayudado a esta poblacion a sobrevivir mediante la reduccion al riesgo de infeccion. Ademas,
hipotetizamos que la distribucion de A. varius pudo haber cambiado en los ultimos 50 anos, penetrando mas
alto en las regiones montanas de la cordillera de Talamanca, un cambio en la distribucion que también podria
Correspondence. ':* andresjmo@gmail.com ORCID: 0000-0002-8787-0820; !?° fmontoya@yorku.ca ORCID: 0000-0002-8273-5515;
‘federico. bolanos@ucr.ac.cr ORCID: 0000-0002-7935-64 18; °° gilbert.alba@gmail.com ORCID: 0000-0001-8418-043X
Amphib. Reptile Conserv. 115 October 2019 | Volume 13 | Number 2 | e192
New Atelopus varius population in Costa Rica
estar ayudando con su supervivencia a ciertos factores ambientales. Con el descubrimiento de una nueva
localidad para A. varius, nuestro estudio ofrece un argumento de comportamiento animal para explicar la
recuperacion de especies, asi como una posible expansion de lo que se ha aceptado como la distribucion
historica de esta especie.
Palabras clave. Ate/opus varius, historia natural, ciencia citudadana, reaparicion de especies amenazadas, rana arle-
quin, hongo quitrido, Corredor Biolégico Alexander Skutch, Costa Rica
Citation: Jiménez-Monge A, Montoya-Greenheck F, Bolafios F, Alvarado G. 2019. From incidental findings to systematic discovery: locating and
monitoring a new population of the endangered Harlequin Toad. Amphibian & Reptile Conservation 13(2): [General Section]: 115-125 (e192).
Copyright: © 2019 Jiménez-Monge et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 14 September 2018; Accepted: 16 July 2019; Published: 23 October 2019
Introduction
Over 75% of the species in genus Ate/opus are assessed
as “Critically Endangered” by the International Union
for the Conservation of Nature Red List (IUCN 2015).
Within this genus, the Harlequin Toad (Ate/opus varius,
in Spanish as “Rana Harlequin”), 1s the last remaining
species in Costa Rica. The other three representatives are
believed to be extinct (Barrio-Amoros and Abarca 2016).
This moderately-sized toad 1s associated with small,
fast-moving streams, where it is found along the banks
and sitting on rocks in the stream. Endemic to Costa
Rica and Panama, at one point there were over 100
known populations in both the Atlantic and Pacific Slope
versants of the mountain ranges in Costa Rica and western
Panama, reaching up to 2,000 m asl (Savage 2002). In
the mid-1990s, A. varius was believed to be extirpated
from Costa Rica, following a drastic decline that began
in Monteverde in 1988, where it remains absent (Pounds
and Crump 1994). Apart from habitat loss, two other
leading possible explanations for the Harlequin Toad’s
disappearance are climate variations and fungal disease.
Research so far suggests the possibility that the decline
of A. varius has a multifactor explanation (Pounds et
al. 2010; Berger et al. 1998) combining both the effect
of climate stress and the appearance of the fungus
Batrachochytrium dendrobatidis (Bd).
Since its loss during the 1990s, four known re-
discoveries of the species have been documented, each
in private properties in the Pacific slope in Puntarenas
Province, Costa Rica. In 2003, a population was
discovered at Fila Chonta, Quepos (Pounds et al. 2010;
Ryan et al. 2005). Nine years later, to the South, a new
breeding population was found near Las Tablas, near
the Panamanian border, at 1,300 m asl (Gonzalez-Maya
et al. 2013). One individual of A. varius was reported
near Buenos Aires, at an elevation of 840 m asl (Solano-
Cascante et al. 2014). Moreover, there was a recent
rediscovery of A. varius by Barrio-Amoros and Abarca
(2016) at 400 m asl in a rocky stream located in the Uvita
Region. Those authors observed nine adult males, one of
which was dead. They tested two live individuals and the
one dead specimen for Bd, and the dead specimen was
the only one to test positive for Bd (Barrio-Amoros and
Abarca 2016).
The pattern of previous reappearances of this species
has been unclear. In some cases, it appeared in small
Amphib. Reptile Conserv.
secluded creeks (Barrio-Amoros and Abarca 2016), and
in others, it appeared in large, open, and fast flowing
rivers (Gonzalez-Maya et al. 2013; Solano-Cascante et
al. 2014), and at altitudinal ranges from almost sea level
to as high as 1,500 m asl. The sites identified thus far
are all on the Pacific slope, amid degraded landscapes
in unprotected land and fragmented, isolated conditions.
This pattern of reappearance makes these populations
highly vulnerable to habitat loss and environmental risks,
such as the population at one of the known localities in
Costa Rica which is under serious threat of landslides
(Pounds et al. 2010).
Here a newly discovered population of A. varius is
presented, found in the Alexander Skutch Biological
Corridor (ASBC), in the Pacific Slope foothills of La
Amistad International Park. We present crucial natural
history remarks and evaluate the presence of Bd infection
in this population. The natural history of amphibian
species can hold important clues for their survival, given
that the effect of fungal infection can be modified by the
host’s ecology, behavior, and life history (Woodhams
et al. 2008). The exact location of the site 1s withheld,
given that the protection of such sensitive information
is of utmost importance in the case of A. varius in Costa
Rica. All the re-discovered populations are outside of
national protected areas and hence are highly susceptible
to commercial trade, collection, and the irresponsible
handling that can lead to a decrease in population
or increased risk of disease. The IUCN guidelines
acknowledge this risk regarding sensitive data access and
the publishing of data that identify specific geographic
locations IUCN 2012).
Materials and Methods
The ASBC extends over 6,012.60 ha (Fig. 1) within the
canton of Pérez Zeledon in the province of San José. The
principal communities of the ASBC include Quizarra,
Santa Elena, Montecarlo, San Francisco, San Ignacio,
Santa Marta, Santa Maria, and Trinidad. The ASBC
lies between 650 and 1,650 m asl and contains the first
remnant population of A. varius outside the province of
Puntarenas.
Note that the findings documented by community
members and students of the Faculty of Environmental
Studies of York University were essential in locating this
population of A. varius. The incidental sightings came
from at least three separate locations along two different
October 2019 | Volume 13 | Number 2 | e192
Jimenez-Monge et al.
GHIRRIPO PAGIFICO
9.400
Key
[) Chirripé National Park
(9) Las Nubes Biological Reserve
GH Alexander Skutch Biological Corridor
GB Los Cusingos Bird Sanctuary
MM Core Corridor
— Rivers
® Towns
Elevation
Ml 500
m™) 1000
1500
2000
Me 2500
QUEBRADA\GHANGHOS
-83.600
Fig. 1 Location and boundaries of the Alexander Skutch Biological Corridor (ASBC) in the province of San José, Costa Rica.
rivers. The rivers are at least 2.3 km apart in a straight
line and separated by mountainous formations. Some
observers had seen toads along the same river, but the
sightings were 300 m apart. In-depth interviews were
conducted with the observers of the Harlequin Toad
incidental sightings to locate the population. After the
interviews, 18 survey days followed, during which over
65 hrs were spent locating, observing, and sampling A.
varius in the previously identified locations.
The interviews aimed to determine as accurately as
possible the location, date, time, available GPS data
(geo-tracking in mobile devices), weather, and relevant
information of each sighting. In April and June 2016,
two visits to the narrowed-down sites were conducted
and systematic searches were performed. These included
six independent diurnal explorations ranging from 3-5
h each, mostly starting at 7:00 AM, with night surveys
also conducted to try to find individuals sleeping in the
foliage. These visits were not successful in locating any
individuals of the population. However, in February
2017, another search successfully located the area
where A. varius resides. After the first individual was
encountered, a transect of 1.1 km was established to
monitor the identified locality systematically.
The transect was surveyed continuously for six days
in February 2017, nine days in June 2017, and three
days in January 2018. These months were selected to
account for seasonal variation, in order to increase the
chances of an encounter. Systematic surveys started early
in the morning and lasted for an average of four h, with
additional surveys carried out sporadically at night to
identify additional locations and sites. The transect was
hiked starting on opposite ends alternatively to account for
possible time variations of activity of the toads. The search
process usually involved 4-6 h of daily effort, walking
along the river and searching in caves, rocks, foliage, and
Amphib. Reptile Conserv.
vegetation above the river. Upon encountering the toads,
they were swabbed for Bd samples, and individuals were
measured and photographed both dorsally and ventrally.
Upon the conclusion of these procedures, individuals
were released in the same location, and each was
handled with a separate set of gloves. Fourteen of these
individuals were sampled for Bd, 10 during the February
2017 surveys and four during June 2017, two of which
were juveniles.
Sex and age were also recorded, along with substrate,
activity (Rest/sleep, Hide, Bask/Splash, Walk/Climb/
Feed), and distance from the river upon first encounter.
For simplicity, the behavior labelled as “splash” refers to
moisture control, as toads absorb water from wet surfaces
in the stream's splash zone (Pounds and Crump 1994).
For better data analysis, the substrate Vegetation was
classified as either trees, bromeliads, branches, or tree
trunks; Soil/Rock refers to either bare ground, crevices,
boulders, or mossy regions on top of the bare rock. The
distance from the river was recorded with horizontal and
vertical distances measured from the water’s edge to the
perch where the toad was found.
The skin swab and storage protocol by Whitfield et
al. (2017) was used, which involves rubbing a sterilized
swab (MW-100 cotton-tipped swab) on the dorsum,
the venter, the sides, and the limbs. Nucleic acids were
extracted from the swabs using Prepman Ultra and Real-
Time PCR protocols (Boyle et al. 2004; Kriger et al. 2006)
in the Laboratory of Experimental and Comparative
Pathology, School of Biology, University of Costa Rica.
Positive and negative controls were run in triplicate on
each 96-well PCR plate. Bd primers and probes (Boyle
et al. 2004) were used in a TaqMan® Gene Expression
Assay (Applied Biosystems, Carlsbad, California).
Samples were run in an Applied BioSystems Prism 7500
Sequence Detection System in Centro de Investigacion
October 2019 | Volume 13 | Number 2 | e192
New Atelopus varius population in Costa Rica
en Biologia Celular y Molecular (CIBCM), University of
Costa Rica. Samples corresponding to 14 animals from
the study site are described.
Results
Open-ended Interviews of Incidental Sightings
In 2015, two independent incidental sightings of the
Harlequin Toad were documented, photographed, and
reported by local community members of the ASBC to
York University’s LNP Director (FM). In March 2016,
a York University student spotted and photographed
another A. varius specimen in the ASBC. Subsequently,
in August 2016, new sightings of the Harlequin Toad
were further documented by students and community
members. Additional sightings of individuals were also
reported by the Tropical Science Center Los Cusingos
Administrator Mario Mejia for May, August, and
September of 2016. During these two years of incidental
sightings, the authors engaged in open-ended interviews
with the incidental observers to expand on_ their
information. These interviews provided precious data for
reducing the search area and narrowing the times of the
day for targeted searches.
Transect Observations
In February 2017, 13 individuals in a rocky stream
within the identified locations in the ASBC were
photographed and identifying body patterns were noted.
Eleven were males and two were females—no juveniles,
eges, or tadpoles were observed. In June 2017, six new
individuals, identified by their unique body patterns,
were recorded in the same study area—three females
and three juveniles. In August 2017, at least one other
individual was observed. In total, with the transect
observations and the photographed incidental sightings,
at least 25 different individuals have been identified in
these locations. The sites where this population resides
are along a wide, open, and fast flowing river, with a
young riparian forest and some old tall trees, surrounded
by a disturbed landscape, with only 10 to 20 m of riparian
forest habitat in some areas.
Males had an average snout-vent length of 25.7 mm
and females 34.3 mm. Male dorsal patterns appear to
include more yellow and green tones, and females have
a stronger orange and red coloration (see Fig. 2). This
coloration is consistent with the remarks of Savage
(1972) on Atelopus populations of Panama and Costa
Rica. Juveniles, on the other hand, have no red and tend
towards lime green, with patterns that are much more
speckled (Fig. 3C,E). All individuals appeared to be in
good health, and no external lesions were present; in
most cases, the skin was colorful, vibrant, and healthy.
Interestingly, the females had very wrinkly cloaca,
probably due to oviposition; no males exhibited any
similar skin condition. One female was molting (Fig. 2E),
from whom skin samples were collected and observed
under the microscope, which detected no presence of Bd.
In total, 14 individuals were tested for Bd, all of which
tested negative for Bd diagnosis.
Amphib. Reptile Conserv.
Just one-quarter of the identified adults were females,
and males were sometimes observed in groups. There
was no indication of reproduction in February, while
in June, juveniles were located, all of them at least 2 m
above the river and in the foliage. In contrast to other
populations of A. varius, the toads in the ASBC were
mostly located above the riverbed, often found in the
foliage, tree trunks, and bromeliads between 1-6 m
above the water, both during day and night. Of the 37
recorded observations, only 11 individuals were seen
close to the river or the splash area, and 10 of them were
seen in vegetation between 3-6 m high.
Natural History Notes
During the surveys, there was ample opportunity to
observe the natural history of this species, and these
observations can help other scientists better locate and
identify new sites in the field, especially when there are
previously existing reports from community members.
Despite the Harlequin Toad’s bright coloration, this
species can be challenging to locate in the field. For
example, during our systematic exploration, the first
individuals were found after almost 25 h of searching in
the same location where it was later documented.
The start of diurnal activities varied among the
seasons. During the dry season, toads were easily located
very early in the morning; but during the wet season,
toads were less frequent, and surveys needed to start
much later when the day had warmed up. Nineteen
sightings were obtained during January and February, but
only six individuals in June, even though more time and
effort was spent during this month. Overall, the sightings
of females were less abundant, and for both sexes, there
were more individuals seen during the dry season. There
was a change in sex ratio between the two seasons (Fig.
4,G=4.216, 1 df, P=0.040), with proportionately more
males detected during the dry season than the wet season.
Regarding the substrate, females were generally
absent from the leaf litter and mostly found on the
vegetation and river boulders, while males were found
on the leaf litter (Fig. 5, G = 9.035, 2 df, P = 0.011).
Previous records suggest that this toad is most often
found along the banks, sitting on the rocks near the
splash zone (Crump and Pounds 1985; Pounds and
Crump 1994; Savage 2002). However, in this case, adults
were typically found in the vegetation or on the ground,
basking on the rocks or foraging along the river bank,
and rarely seen in the splash zone (Fig. 6). Juveniles had
a stronger preference for vegetation (Fig. 6, G= 8.365, 2
df, P =0.015), which explains why they were so difficult
to locate (Fig. 3E).
The toads were observed basking more during the wet
season, on the rocks near the openings in the canopy or
the exposed vegetation (Fig. 2E-G). For example, the
three females in Fig. 2 are pictured as found: the first was
basking, exposed on the vegetation in an open part of the
river around 9:00 AM during the dry season; the second
and third females were basking on the river rocks during
the wet season. Hiding and basking were activities found
to be significantly associated with the dry season, while
hiding was never seen during the wet season (Fig. 7, G
October 2019 | Volume 13 | Number 2 | e192
Jimenez-Monge et al.
e)
ZA ‘ 1A #
. i f !
' i: "oh
i — "ear. he
’ i ‘
o XL. _— E F ‘ =
Fig. 2 Detail of Atelopus varius individuals found during February and June 2017 in the ASBC. The left column includes males;
the right column includes females. Males (B) and (C) were photographed as found, as were females (E), (G), and (H). Note the
spread-out basking position of female (G).
Amphib. Reptile Conserv. October 2019 | Volume 13 | Number 2 | e192
New Atelopus varius population in Costa Rica
B
Fig. 3 Males, females, and juveniles of Ate/opus varius found in the Alexander Skutch Biological Corridor. (A) Male found during
cm ag ™
F ho % bing
a r
. a ‘ - =
ee - sg
=
February surveys. (B) Sleeping male in the leaf litter in the same location of a male in Fig. 2(A). (C) and (E) are juveniles high
above the river bank, at least 3-4 m high in the vegetation of the understory, and juvenile (C) is sleeping. (D) A female Harlequin
Toad sleeping on the vegetation five m above the river.
= 13.159, 1 df, P = 0.004). When rains were abundant,
the toads were found sleeping or resting high on the
vegetation.
A difference in activity patterns was also observed
between males and females of this species (Fig. 8, G
= 15.247, 1 df, P = 0.002). During this study, females
were mostly seen basking on river boulders, or on top
of vegetation above the river; while males were more
passive, with significantly predominant activity in the
leaf litter and crevices of the riverbed, hiding, or resting
(Fig. 3A-B). On the other hand, the activity for juveniles
of this species mostly involved sleeping or active
movement for feeding. Juveniles were never observed
basking or hiding like the adults (Fig. 9, G= 9.934, 1 df,
P=0.019).
The Harlequin Toads studied here seemed to be
very faithful to their sleeping grounds. On five separate
occasions, three individuals, including a juvenile (Fig.
3C), were seen sleeping on the same leaf during the night.
Besides the observed nocturnal feeding behavior, almost
Amphib. Reptile Conserv.
all the individuals seen during the night were sleeping
in the vegetation high above the river. Activity started
before dawn. One of these individuals was monitored
during the night, and its activity started before 4:30 AM.
Toads sleeping high in the vegetation (Fig. 3 C,D) made
their way down to lower levels of the ground as the
morning warmed up, with some of them remaining on
the vegetation during the day (Fig. 2E).
Discussion
Based on Savage’s (1972; 2002) reviews of A. varius
distribution in Costa Rica and Panama, it is clear that
most of the recently re-discovered populations have been
found in areas of their historical distribution. The report
by Ryan et al. (2005) for Fila Chonta, 10 km northwest of
Quepos, matches the premontane distribution suggested
for southwestern Costa Rica, where the nearest site
identified by Savage (1972) is Bart. The account by
Barrio-Amoros and Abarca (2016) for the Uvita region
October 2019 | Volume 13 | Number 2 | e192
Jiménez-Monge et al.
O Female
GO Male
Individuals
Dry Wet
Season
Individuals
Fig. 4 Occurrence of males and females of Atelopus varius according
to season.
16
DAdult
14
DJuvenile
12
2 10
3
are
= 6
4
2
0
Soil/rock Vegetation Leaflitter
Substrate
Fig. 6 Substrate preference of Ate/opus varius according to age.
10
Ol Female
8 G Male
x
& 5
so
2
= 4
2
0
Rest/sleep Hide Bask/Splash Walk/Climb/
Feed
Activity 7
Fig. 8 Activity pattern of Ate/opus varius according to sex.
matches with that reported by Savage (1972); and finally,
the rediscovery in Las Tablas by Gonzalez-Maya et al.
(2013), brings hope for the survival of the toads near
Coton, also previously identified by Savage (1972).
These findings confirm that some populations in the
Pacific versant have managed to escape the decline while
persisting in the same localities, at least so far. However,
evidence from our research, with the discovery of a new
locality, offers augmented hope for species recovery. We
hypothesize that the behavior of this population could
have helped to reduce the risk of exposure to Bd infection
and also to allow a possible change in the historical
distribution of this species.
These results, and the similarity between both
the scientific and community accounts discussed
below, suggest that A. varius distribution could have
Amphib. Reptile Conserv.
Individuals
OrRFNW HU DN WO WO
Individuals
121
12
10
O Female
G Male
Soil/rock Vegetation Leaflitter
Substrate
Fig. 5 Substrate preference of Ate/opus varius according to sex.
pany
io)
O Dry
O Wet
Rest/sleep Hide Bask/Splash Walk/Climb/
Activity Feed
Fig. 7 Activity pattern of Atelopus varius according to season.
O Adult
GB Juvenile
8
6
4
2
0
Rest/sleep Hide Bask/Splash Walk/Climb/
Activity eat
Fig. 9 Activity pattern of Atelopus varius according to age.
changed to penetrate higher in the montane regions of
the Talamanca Mountain Range in the Pacific Slope.
Despite the lack of specimens for the area and the lack
of a collection archive, previous evidence has recorded
A. varius, specifically this ecomorph, in the San Isidro
del General region at 704 m asl (Savage 1972), with no
other accounts found by the authors for the ASBC area
(from 1,100—1,500 m asl). Furthermore, Savage (1972)
refers to this toad as a predominantly premontane frog
with penetration into lower montane zones only at six
localities in Costa Rica, none of which includes the
area of this study—the closest area identified is Pérez
Zeledon at 704 m asl (Savage 1972). Taking Savage’s
(1972) account into consideration, the discovery of this
population in montane areas of the ASBC suggests this
is an undocumented locality. This scientific account is
October 2019 | Volume 13 | Number 2 | e192
New Atelopus varius population in Costa Rica
congruent with interviews of highly experienced locals
who do not report or remember this species being present
at elevations higher than 600—700 m asl.
Long-time residents of what is now the Alexander
Skutch Biological Corridor remembered that the
Harlequin Toad had been abundant in the area some
50 years ago, but that this toad had not been reported
again for decades, until now. During initial interviews,
local observers showed good competency to immediately
identify Harlequin Toads. One of them acknowledged the
remarkable altitudinal change for this species over the
years, “this frog was very common at 600 m over twenty
years ago, now it is over 1,000 m. It was never here, and
it has come higher in the mountain. It’s the first time
I see it again in all these years” (Ramon Mora). This
citizen testimony along with Savage’s (1972) account
could point to a possible geographic displacement. When
considering the possible displacement, we acknowledge
that reduced biodiversity exploration in the area could
explain how this population went under the scientific radar
for so long; yet, with no valid reason, this assumption
would disregard the confidence, skills, experience, and
traditional knowledge of the inhabitants that are quite
confident the frog was not present over 700 m asl in the
past. If this species were not so easily identified, with
such a reduced risk of misidentification in the field, we
would consider this possibility. This possible change in
distribution might be helping to facilitate its continuing
survival through some environmental stressors, such as
climate change and habitat loss. It might also increase the
risk of Bd exposure, and clearly more research is needed
to corroborate this possible explanation, exploring the
trade-offs between adaptation to environmental changes
and Bd exposure.
The reappearance of A. varius in this region could
be the result of several possible factors. One hypothesis
is that establishing the biological corridor in 2005, and
subsequent efforts to enhance ecological connectivity
between forest patches, have allowed for the recovery
of habitats that previously served as niches for relict
populations on the verge of extinction, allowing those
populations to recover and relocate, possibly pushed by
environmental changes. Another potential explanation
has to do with the possible emergence of resistance
among these threatened relict populations of A. varius
to the previously devastating Bd fungal disease (Perez
et al. 2014).
To expand on the emergence of resistance to the Bd
infection hypothesis, we present two critical remarks that
contribute to the natural history of the species and might
be related to this population’s survival. First, the toads
in the area are seen less often on the splash region of
the river, and more often on the vegetation, regardless
of seasonality. Second, the typical sedentary behavior
in the mossy rocks near the splash zone associated with
this species (Pounds and Crump 1994) is not as typical in
this location. The toads are not so sedentary, and basking
seems to be more important here than capturing moisture
in the splash zone. Many authors, including Pounds and
Crump (1994), recognize that this species depends on
the moisture of the splash zone and individuals tend to
ageregate in the waterfall splash with the progression
Amphib. Reptile Conserv.
of the dry season. The experiences of working with this
population complement this information. Here, toads
are regularly seen in the foliage, tree trunks, and the leaf
litter, and not on the splash zone, only seven of the 37
registered encounters were found on the river rocks or
crevices. The basking behavior 1s as important, or perhaps
more so, than moisture-seeking behavior. The toads
appear to move to open areas on the river bank or the
exposed vegetation where there is more solar radiation;
and the selection of such areas was more frequent during
the warmest time of the morning, especially on colder
days. This selection could also explain the difference of
activity during dry and wet seasons, where during the
wet season the toads were “lazier” in the early hours of
the morning when it was cold and they were found closer
to the river when the day was warmest. These individuals
were much less sedentary than previously reported,
engaging in significant daily movements. Anurans
sleeping on the vegetation 3-4 m above the river move
during the morning down to the river bank; explaining
why this species has been hard to locate in the area, as
researchers might focus solely on crevices, rocks, and
roots as reported by most of the literature. Understanding
this was the key to finding the juveniles that were far
from the river and much higher than eye-level.
In other words, the natural history remarks noted
above suggest that A. varius spends less time closer to
the river and more time in open areas basking; which
in turn might be linked to available solar radiation and
moisture control. Temperature (Woodhams et al. 2003)
and moisture (Johnson et al. 2003) have been suggested
as two important environmental factors influencing the
growth and survival of B. dendrobatidis. So this behavior
could explain why this toad survived in an area cataloged
as highly likely for the existence of Bd (Puschendorf et
al. 2009). Furthermore, the negative results of the Bd test
support this theory. The documented absence of infection
in these Harlequin Toads, a highly susceptible species in
an area identified with a high probability for occurrence
of Bd, allows us to hypothesize that spending less time
closer to the river and more time in open areas basking,
could help the toads of this population survive by
reducing infection risk. The findings of Woodhams and
colleagues (2003) support our hypothesis; they present
evidence that short periods of high body temperature can
eliminate the pathogen from its hosts, with experiments
suggesting that normal thermoregulation can clear frogs
of chytrid infection (Woodhams et al. 2003). We hope
this account can help provide a better understanding of
the behavior of Ate/opus, as this behavior might hold
clues for the frog’s resistance to Bd or climatic changes,
and can also help to locate new populations.
Conclusions
Garcia-Rodriguez et al. (2012) ask “Where are the
survivors [of] relict populations of endangered frogs
in Costa Rica?” In this research, both community
members and scientists have contributed to answering
this question. Moreover, with A. varius being among the
most endangered of all amphibian species (La Marca et
al. 2005), it is certain that the discovery of the Harlequin
October 2019 | Volume 13 | Number 2 | e192
Jimenez-Monge et al.
Toad in the Alexander Skutch Biological Corridor makes
the conservation efforts in this biological corridor of
critical importance. This population is_ particularly
relevant because of ongoing attempts by private
companies to obtain permits for building a hydroelectric
plant that would dam the two major streams in the ASBC,
destroying the habitats successfully recovered during
a decade of conservation efforts in the corridor. The
reappearance of the Harlequin Toad, currently classified
as Critically Endangered (IUCN 2015), lends supporting
evidence to the effectiveness of this habitat recovery.
The active involvement of citizens in the discovery
of A. varius in the ASBC points to the importance of
strengthening the citizen science component to further
the knowledge base regarding this and other species in the
area. The historical role of citizen science in ecological
research has been generally overlooked, despite its
significant contributions (Miller-Rushing et al. 2012;
Dickinson et al. 2012). The opportunistic and widespread
nature of these sightings suggests that strengthening
citizen science approaches can help to maximize
resources and opportunities for encountering this and
other rare, endangered species. Citizen science creates a
nexus between science and education that expands the
frontiers of ecological research and public engagement
(Newman et al. 2012). After all, without the enthusiastic
and curlosity-filled reports from the community, the re-
emergence of this rare and endangered species might have
gone completely undetected by the scientific community.
Moreover, this participatory process can generate new
meanings and values for herpetofauna in the community,
leading to improved human behaviors directed at the
protection of these and other vulnerable species.
In addition to continuing to monitor for the presence of
A. varius in the ASBC, the community initiative that has
already documented the reappearance of the Harlequin
Toad in the biological corridor will also be useful in
providing further data to help answer pending questions
regarding the impacts of climate change, fungal disease,
and pesticides on these fragile populations.
Acknowledgments.—We thank community members
Hans Homberger, Ramon Mora (“Monchito”), Mario
Mejia, Byron Valverde, Walter Arias, and Christian Arias
for their citizen contributions; and Luis Angel Rojas
for logistical support in the field. We are also grateful
to York University Faculty of Environmental Studies
graduate students Stephanie Butera and Carmen Umafia
for sharing their documented sightings; and to the Fisher
Fund for Neotropical Conservation, for financial support
to the Las Nubes Project. We also thank the private,
anonymous donors that supported the research conducted
by AJM and his graduate degree: your support helped
make this possible. Finally, we would like to recognize
the support of Gerardo (Cachi) Chaves for the creation of
the Alexander Skutch Biological Corridor map presented
in this publication.
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Jimenez-Monge et al.
Andrés Jiménez Monge is a biologist from the Universidad de Costa Rica (San
José, Costa Rica) with a Master’s degree in Environmental Studies, and a Diploma
in Business and Sustainability from York University (Toronto, Ontario, Canada).
Currently, Andrés is working with Bird Studies Canada as Urban Program Coordinator.
His research fields include organizational behavior, change management, conservation,
and herpetology. Andrés strives for creating connections between people and the
planet; find more of his work at http://www.razaverde.com and http://www.udemy.
com/birdwatching.
Felipe Montoya-Greenheck has a B.S. in biology from the University of New Mexico
(Albuquerque, New Mexico, USA), a Master’s degree in tropical ecology from the
Universidad de Costa Rica (San José, Costa Rica), and a Ph.D. from the University
of New Mexico. Currently, Felipe is the director of the Observatorio del Desarrollo,
a research center of the University of Costa Rica, and the director of the Las Nubes
program of the Faculty of Environmental Studies at York University (Toronto, Ontario,
Canada). His research fields include environmental anthropology, rural development,
conservation, and wellbeing.
Gilbert Alvarado is a Costa Rican biologist of the Universidad de Costa Rica (UCR).
Gilbert completed his studies as a veterinarian from Universidad Nacional de Costa
Rica (UNA), and his master's studies in the Regional Postgraduate Program in Biology
of the UCR. He is currently developing his doctoral studies in the Experimental and
Comparative Pathology Program of the Faculty of Veterinary Medicine and Animal
Sciences, University of Sao Paulo, Brazil, in the Laboratory of Wildlife Comparative
Pathology, sponsored by the Office of International Affairs and the UCR. Gilbert was
a professor of Pathology and Anatomy at the UNA, and he has been a professor of the
Section of Zoology and researcher of the School of Biology of the UCR. He has been a
researcher at the Research Center for Microscopic Structures from 2013-2014; as well
as the veterinary adviser of the Biological Testing Laboratory in 2015; both academic
units of the UCR. As principal investigator and collaborator, Gilbert has developed
different projects within his fields of interest (comparative pathology of wildlife, host-
pathogen relationships, amphibian diseases, and conservation of critically endangered
Species), and served as regent and veterinary adviser in herpetofauna centers. He is
founder and coordinator of the Laboratory of Experimental and Comparative Pathology
of the School of Biology, UCR.
Federico Bolafios has done master’s studies at the Postgraduate Regional Program
in Biology in Universidad de Costa Rica. Currently, Federico is a professor and
researcher at the Biology School in the same institution and curator of the Herpetology
Collection of the Zoology Museum. Federico’s research is in the fields of conservation,
systematics, ecology, and behavior of amphibians and reptiles, but his publications deal
mainly with the first topic.
125 October 2019 | Volume 13 | Number 2 | e192
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 126-132 (e193).
Thorius narismagnus (Amphibia: Plethodontidae):
rediscovery at the type locality and detection of a
new population
‘José L. Aguilar-Lopez, ?*Paulina Garcia-Banuelos, *Eduardo Pineda, and *Sean M. Rovito
'23Red de Biologia y Conservacion de Vertebrados, Instituto de Ecologia, A.C., Carretera antigua a Coatepec 351, El Haya, Xalapa, Veracruz,
MEXICO *Unidad de Genémica Avanzada (Langebio), Centro de Investigacion y de Estudios Avanzados del Instituto Politécnico Nacional, km 9.6
Libramiento Norte Carretera Irapuato-Leon, Irapuato, Guanajuato CP 36824, MEXICO
Abstract.—Of the 42 Critically Endangered species of plethodontid salamanders that occur in Mexico, thirteen
have not been reported in more than ten years. Given the lack of reports since 1976, the minute plethodontid
salamander Thorius narismagnus is widely considered as missing. However, this report describes the
rediscovery of this minute salamander at the type locality (Volcan San Martin), as well as a new locality on Volcan
Santa Marta, 28 km southeast of its previously known distribution, both in the Los Tuxtlas region of Veracruz,
Mexico. The localities where T. narismagnus has been found are mature forests in a community reserve on
Volcan San Martin and a private reserve on Volcan Santa Marta. The presence of maxillary teeth, generally
absent in Thorius, are reported here in some T. narismagnus females. Two efforts which may contribute to the
conservation of Thorius narismagnus are the preservation of the cloud forests where this species persists, as
well as the determination of the presence and possible effect of chytrid fungus in these populations.
Keywords. Conservation, ecological reserve, Los Tuxtlas, missing species, minute salamander, molecular analysis,
Mexico
Citation: Aguilar-L6pez JL, Garcia-Bafuelos P, Pineda E, Rovito SM. 2019. Thorius narismagnus (Amphibia: Plethodontidae): rediscovery at the type
locality and detection of a new population. Amphibian & Reptile Conservation 13(2) [General Section]: 126-132 (e193).
Copyright: © 2019 Aguilar-Lépez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 1 October 2018; Accepted: 4 August 2019; Published: 8 November 2019.
Introduction
In Mexico, 132 species of plethodontid salamanders
have been recorded (AmphibiaWeb 2019), 42 of which
are Critically Endangered (CR) according to the Inter-
national Union for the Conservation of Nature (IUCN
2019). This conservation status may be assigned due to
various combinations of biological characteristics (e.g.,
restricted distribution or specific environmental require-
ments) and risk factors (e.g., habitat modification or
climate change; Stuart et al. 2008). In recent decades,
population declines have been observed or estimated for
several species (Frias-Alvarez et al. 2010) and in some
cases, despite intensive search efforts, finding them has
not been possible.
According to the IUCN (2019), 13 Critically Endan-
gered plethodontid species in Mexico have not been re-
ported in more than 10 years. Since 2010, six of these
species have been rediscovered: [sthmura naucampate-
pet! (Naturalista 2019), Chiropterotriton magnipes, C.
mosaueri, Pseudoeurycea ahuitzotl, P. tlahcuiloh, and
Thorius munificus (AmphibiaWeb 2019). However, so
far there have been no subsequent records of the remain-
ing seven species, including Thorius narismagnus. The
unknown status of these species highlights the need to
carry out sampling efforts in their historical localities
and to explore those areas with favorable environmental
conditions, in order to locate new populations (Sandoval-
Comte et al. 2012).
Thorius narismagnus (Shannon and Werler 1955)
is a minute salamander with a known distribution that
comprises only four localities, not more than 8 km apart,
on Volcan San Martin in the Los Tuxtlas region, Veracruz,
Mexico (Fig. 1), in an elevational range between 890
and 1,200 m asl (Hanken and Wake 1998). Thorius
narismagnus is considered as CR because the extent of
its occurrence is < 17 km? with reductions in the extent
and quality of its habitat, and due to a continuing decline
in the number of mature individuals (IUCN 2016).
The historical records of 7? narismagnus include 55
specimens collected between 1953 and 1976, and since
Correspondence. ! jal. herp@gmail.com, »-* paulinabanuelos@hotmail.es, *eduardo.pineda@inecol.mx;
+ sean.rovito@cinvestav.mx
Amphib. Reptile Conserv.
November 2019 | Volume 13 | Number 2 | e193
Aguilar-Lopez et al.
United States of America
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gine og es
aay
Gulf of Mexico a
18°20'N 18°30'N 18°40'N
18°10'N
95°20'W 95°10'W
\
Mexico
Elevation (m)
[my 0-300
[i 301-600
fm 601-900
fy 901-1200
By 1201-1500
[>] 1501-1800
95°W 94°50'W 94°40'W
Fig. 1. Locations of historical collection localities and the new localities of Thorius narismagnus in Los Tuxtlas region, Mexico.
then this species has not been reported (IUCN 2016).
Rediscovery
As part of a study on the diversity and conservation
of amphibians in Veracruz, fieldwork was carried out
in a cloud forest in the community reserve Ejido Ruiz
Cortines, San Andrés Tuxtla, Veracruz (18°32'53"N,
95°09'16" W; 1,136 m asl) on Volcan San Martin (Fig. 1;
Fig. 2A) and in the private Ecological Reserve "La Otra
Opcion" Catemaco, Veracruz (18°22'32"N, 94°55'28"W;
1,075 m asl) on Volcan Santa Marta (Fig. 1; Fig. 2B).
At both sites searches for amphibians (08:00—12:00
and 20:00—00:00 h) were conducted in all terrestrial
microhabitats commonly used by these organisms
(Crump and Scott 1994).
In the Ejido Ruiz Cortines community reserve,
with a cumulative search effort of 72 person-hours in
September 2012, three individuals of the genus Thorius
were detected, two of which were collected (from which
a tissue sample was taken and the individuals were
subsequently preserved) and deposited in the Coleccion
de Anfibios y Reptiles del Instituto de Ecologia A.C.
(CARIE 0857, 1137; Fig. 2C). A sampling effort of 24
person-hours was carried out in July 2015 at this locality,
but there were no sightings of any minute salamanders.
The two collected specimens measured 17.6 and 11.4
Amphib. Reptile Conserv.
mm in SVL, the ratios between the length and width of
the nostrils were 1.14 and 1.09, with four and five free
intercostal grooves separating the adpressed fore and
hind limbs, respectively.
In the private ecological reserve La Otra Opci6on, with
cumulative search efforts of 96 person-hours in July 2015
and 66 person-hours in July 2017, three individuals of
Thorius were detected in well-preserved forests in each
year. The three individuals detected in 2015 were captured
(each one was measured and a sample of tail tissue was
taken) and subsequently released; these specimens had
SVL measurements of 15.4, 15.9, and 19.4 mm. The
three individuals found in 2017 were collected (CARIE
1251, 1258, 1259; Fig. 2D) and a sample of tissue was
taken from each; they measured 19.9, 22.5, and 21.2 mm
SVL, respectively. The proportions between the length
and width of the nostrils were 1, 1, and 1.15, respectively,
with 5.5 free intercostal grooves separating adpressed
limbs. Two females from La Otra Opcion (CARIE 1251
and 1259) had eight and five maxillary teeth, respectively,
while the adult male (CARIE 1258) lacked maxillary
teeth.
Identification of Specimens
The coloration in life of the specimens collected in the
Volcan San Martin and Volcan Santa Marta localities
November 2019 | Volume 13 | Number 2 | e193
Thorius narismagnus rediscovery in Mexico
ee
Fig. 2. Habitat in the Volcan San Martin locality (A) and a specimen (C) collected from it in life (CARIE 0857). Habitat in the
—
. x, -
oe, ~ - . .
: _ * “he? -s - 1E os + & er .
Volcan Santa Marta locality (B) and a specimen (D) collected from it in life (CARIE 1251).
was light brown with a dark brown spike pattern in the
dorsum, dark brown color on the sides and a dark venter
with small white spots (Fig. 2C, 2D). With the exception
of the presence of maxillary teeth in two females, the
morphological characters and the coloration coincide
with the diagnosis proposed by Shannon and Werler
(1955) and Rovito et al. (2013) for Thorius narismagnus.
Although maxillary teeth are absent in most species of
Thorius, they are present in several species, including
T! smithi, which is relatively closely related to 7
narismagnus. Furthermore, at least two species (7.
grandis and T. omiltemi) have maxillary teeth present
only in females, and maxillary teeth are more common
in females of 7? minydemus than in males, which rarely
have them (Hanken and Wake 1998; Hanken et al. 1999).
Maxillary teeth were absent in a total of 18 specimens
from the type locality of 7) narismagnus on Volcan San
Martin as reported by Shannon and Werler (1955) and
Hanken and Wake (1998), suggesting that they do not
occur in either sex at that locality.
In order to confirm that both populations belong to
Thorius narismagnus, DNA was extracted from liver
tissue of one specimen from Volcan San Martin (the type
locality of TZ. narismagnus) and two specimens from
Volcan Santa Marta using a salt extraction protocol. A
Amphib. Reptile Conserv.
784 bp fragment of the cytochrome b gene was amplified
using primers MVZ15 and MVZ16 (Moritz et al. 1992).
PCR consisted of an initial denaturation step of 94 °C for
2 min, followed by 35 cycles of denaturation at 94 °C
for 30 sec, annealing at 48 °C for 1 min, and extension
at 72 °C for 1 min, with a final extension at 72 °C for 7
min. PCR products were purified using ExoSAP IT (USB
Corporation, Cleveland, Ohio, USA) and sequenced
using the BigDye v3.1 terminator cycle sequencing kit
(Applied Biosystems, Foster City, California, USA) on
an ABI 3730 capillary sequencer. Sequences were edited
using Geneious v8.1.8 (BioMatters, Auckland, New
Zealand), and sequences used in analysis were 750 bp
long after removing low-quality bases. Sequences for
other species of Thorius were obtained from GenBank
and sequences were aligned using Muscle v.3.8 (Edgar
2004). The pairwise GTR distance between sequences
from the two populations was calculated using PAUP
v4.165 (Swofford 2003). Sequences are deposited in
GenBank (Table 1).
The average pairwise divergence for cytochrome b
(cytb) between the two populations was 1.4% (Table
1). This level of divergence is comparable to, or lower
than, that seen between conspecific populations of
various species of Thorius. Several species of Thorius
November 2019 | Volume 13 | Number 2 | e193
Aguilar-Lopez et al.
Webi. 5
accession
mczai48745 | kcssaovs | 9.8 | 10.6] 12.0| 16.0| 73 | 160] 5.0 [19.5] 9.0 {1621 18.6] 13.7] 23.2| 19.0] 17.7] 17.7] 177] 12.5] 65 [103] 173] 59 | 68 |iss{ix0]i90] 66 | 51 fisstiz3| - | |
onus
Sonus
sicaudus
T. insperatus
T. maxillabrochus
T. minutissimus
T. lon
T. pennatulus
T. dubitus
T. lunaris
T. tlaxiacus
Be
coed Mhoen!
Amphib. Reptile Conserv. 129 November 2019 | Volume 13 | Number 2 | e193
3 | T. pulmonaris
3
4
2
1
eae
2
Table 1. Percentage of average pairwise divergence for cytochrome b between the populations of Thorius species in GenBank.
Thorius narismagnus rediscovery in Mexico
from Oaxaca, including 7’ boreas, T. macdougalli, and
T. narisovalis, have substantially higher divergence
than that seen between the two populations from Los
Tuxtlas that were sequenced here. For example, two
populations of Thorius boreas separated by only 17 km
are 5% divergent for cytb (Rovito et al. 2013). The close
genetic similarity between the populations from Volcan
Santa Marta and from the type locality of Volcan San
Martin strongly suggests that these two populations are
conspecific.
Conservation Implications
The record from the Ejyido Ruiz Cortines community
reserve locality represents the rediscovery of T.
narismagnus, 36 years after the last reported record
(Hanken 1976: MVZ183028—-183035) at the type
locality on Volcan San Martin (Hanken and Wake 1998).
Additionally, the record from Volcan Santa Marta extends
the distribution range of this species 28 km southeast of
the closest known locality (Fig. 1). Because the specimens
reported here were found in primary vegetation, and
Diaz-Garcia et al. (2017) recorded 7. narismagnus
in mature forest but not in restoration areas and cattle
pasture in “La Otra Opcion” this species is probably not
able to survive in disturbed forest or even in moderately
disturbed forest. Of the other missing species that the
authors have found recently, only one (7) munificus)
was found in small, highly disturbed forest fragments
and within San Juan del Monte state reserve (Juarez-
Ramirez et al. 2016), while Chiropterotriton magnipes
and C. mosaueri were found in a cave in a national park
with only light to moderate habitat disturbance, and
Pseudoeurycea ahuitzotl and P. tlahcuiloh were found in
intact montane forest (AmphibiaWeb 2019).
To more fully understand the conservation status of
T. narismagnus, an exhaustive sampling effort through
time is needed to determine how the encounter rate of
this species varies throughout the year and whether it is
currently an uncommon species, and to obtain a more
accurate estimate of the population size. Extensive
fieldwork is also necessary in those areas with favorable
environmental conditions on both volcanoes to determine
the full distribution of this species. The extent of well-
preserved forest on Volcan San Martin is ~100 km?, while
on Volcan Santa Marta it is ~185 km? (INEGI 2016).
In addition, determining the presence of the chytrid
fungus Batrachochytrium dendrobatidis (Bd) and its
possible effect on the survival of these 7? narismagnus
populations is critical, because the presence of Bd in Los
Tuxtlas region has been confirmed (Mendoza-Almeralla
et al. 2015) and this pathogen is suspected of being linked
to the population declines of this species (IUCN 2016).
The presence of Bd has been reported in geographically
close species from Central Veracruz, such as Bolitoglossa
rufescens, Aquiloeurycea cephalica, and P. firscheini
(Van Roo et al. 2011), as well as P. nigromaculata
Amphib. Reptile Conserv.
and Thorius pennatulus, for which the presence of the
pathogen has been associated with declines in their
populations (Cheng et al. 2011).
Finally, the finding of two populations of a Critically
Endangered salamander species that has gone unrecorded
for almost four decades highlights the importance of
community and private reserves for harboring species in
imminent danger of extinction. Although both reserves
are relatively small (less than 200 ha) compared to
the Los Tuxtlas Biosphere Reserve in which they are
located, most of the land of these reserves is conserved
forest surrounded by modified environments. In that
sense, this work shows the complementarity between
the governmental and non-governmental reserves for the
protection of species at risk of extinction (see Garcia-
Bafiuelos et al. 2019), particularly those species with
restricted distributions and sensitivity to environmental
disturbances.
Acknowledgements——We are grateful to Ricardo
Luria, Luis Carrillo, Aristides Garcia, Juan Diaz, David
Gonzalez, and Rogelio Agapito for fieldwork support; and
to Ismael Guzman for initial molecular analysis. Wesley
Dattilo provided helpful suggestions that improved this
manuscript. Scientific collection permits were issued by
Secretaria del Medio Ambiente y Recursos Naturales
(SGPA/DGVS/03665/06 and SGPA/DGVS/03444/15).
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Thorius narismagnus rediscovery in Mexico
José L. Aguilar-L6pez was born in Mexico, and obtained his Bachelor’s degree at
Benemeérita Universidad Autonoma de Puebla (BUAP), and his M.Sc. degree at the
Instituto de Ecologia, A.C. (INECOL), both in Mexico. José recently obtained his Ph.D.
degree at INECOL, and he is interested in the diversity, ecology, and conservation of
amphibians and reptiles in tropical environments.
Paulina Garcia-Bafiuelos is a biologist, and recently obtained her Ph.D. degree at the
Instituto de Ecologia, A.C. (INECOL) in Xalapa, Veracruz, Mexico. Paulina obtained her
M.Sc. degree at the Instituto de Neuroetologia at the Universidad Veracruzana, the same
university where she obtained her Bachelor’s degree. She is interested in the current status
and conservation of the plethodontid salamanders of Mexico.
Eduardo Pineda obtained his Bachelor’s degree at the School of Sciences at the
Universidad Autonoma del Estado de México (UAEM) and his doctoral degree at the
Instituto de Ecologia, A.C. (INECOL), in Xalapa, Mexico. Eduardo’s research in the
INECOL is focused on understanding the relationship between the transformation of
tropical forests and biodiversity at different spatial scales, recognizing the importance of
conserved areas and modified habitats for maintaining the diversity of amphibians, and
assessing the current status through fieldwork of amphibian species that are in imminent
danger of extinction. Currently, Eduardo has several undergraduate and graduate students
addressing topics on the ecology and conservation of amphibians and reptiles in Mexico.
Sean Rovito is a professor at the National Laboratory of Genomics for Biodiversity
(Langebio, Cinvestav) in Irapuato, Mexico. Sean’s research focuses on diversification,
genomics, and conservation of Neotropical salamanders, particularly the plethodontid
salamanders of Mexico.
132 November 2019 | Volume 13 | Number 2 | e193
Amphibian & Reptile Conservation
13(2) [General Section]: 133-144 (e194).
Official journal website:
amphibian-reptile-conservation.org
urn:lsid:zoobank.org:pub:F6397C2F-00F 4-4885-810A-54D478A5A184
A new glassfrog (Centrolenidae: Hyalinobatrachium)
from the Topo River Basin, Amazonian slopes of the
Andes of Ecuador
14.* Juan M. Guayasamin, '*José Vieira, *Richard E. Glor, and *Carl R. Hutter
'Universidad San Francisco de Quito USFO, Colegio de Ciencias Biologicas y Ambientales COCIBA, Instituto BIOSFERA-USFO, Laboratorio de
Biologia Evolutiva, Campus Cumbaya, Casilla Postal 17—1200-841, Quito 170901, ECUADOR *Tropical Herping, Quito, ECUADOR *Department
of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Lawrence, Kansas, USA *Department of Biology, University
of North Carolina, Chapel Hill, North Carolina, USA
Abstract.—A new species of glassfrog (Centrolenidae) is described from the San Jacinto River, an affluent
of the Topo River, on the Amazonian slopes of the Ecuadorian Andes. The new species, Hyalinobatrachium
adespinosai sp. nov., can be differentiated from all other centrolenids by the combination of its coloration
(transparent peritoneum and pericardium) and vocalization (call duration = 0.38-0.44 s, with 9-13 pulses per
call; dominant frequency = 4,645—5,001 Hz). However, H. adespinosai sp. nov. is morphologically cryptic with
H. anachoretus, H. esmeralda, and H. pellucidum, from which it differs by call traits (in H. anachoretus: call
duration = 0.32—0.37 s, with 5 or 6 pulses per call, dominant frequency = 4,670—4,800 Hz; in H. esmeralda: call
duration = 0.218—0.257 s, tonal call, dominant frequency = 4,739—5,580 Hz; in H. pellucidum: call duration = 0.112—
0.140 s, tonal, dominant frequency = 5,000—5,710 Hz). Biogeographically, the new species is separated from H.
anachoretus by a considerable distance and, also, the Maranon valley. Finally, following IUCN conservation
criteria, the status of the new species is considered as Data Deficient.
Keywords. Amphibia, Anura, Ecuador, Pastaza basin, phylogeny, Tungurahua Province
Resumen.—Describimos una nueva especie de rana de cristal (Centrolenidae) del rio San Jacinto, afluente del
rio Topo, en la vertiente amazonica de los Andes del Ecuador. La especie nueva, Hyalinobatrachium adespinosai
sp. nov., se diferencia de todos los centrolénidos por la combinacion de su coloracion ventral (peritoneo
y pericardio transparentes) y las caracteristicas de su canto (duracion del canto = 0.382-—0.430 s, con 9-13
pulsos por canto; frecuencia dominante = 4,645—5,001 Hz). Sin embargo, es morfologicamente criptica con H.
anachoretus, H. esmeralda y H. pellucidum, especies de las cuales difiere por su canto (en H. anachoretus:
duracion del canto = 0.32-—0.37 s, con 5 or 6 pulsos por canto, frecuencia dominante = 4,670—4,800 Hz; en H.
esmeralda: duracion del canto = 0.218-—0.257 s, tonal, frecuencia dominante = 4,739-—5,580 Hz; en H. pellucidum:
duracion del canto = 0.112-0.140 s, tonal, frecuencia dominante = 5,000—5,710 Hz). Finalmente, siguiendo los
criterios de la UICN, sugerimos que Hyalinobatrachium adespinosai sp. nov. sea ubicada en la categoria de
Datos Insuficientes.
Palabras clave. Amphibia, Anura, Cuenca del Pastaza, Ecuador, filogenia, Tungurahua Province
Citation: Guayasamin JM, Vieira J, Glor RE, Hutter CR. 2019. A new glassfrog (Centrolenidae: Hyalinobatrachium) from the Topo River Basin,
Amazonian slopes of the Andes of Ecuador. Amphibian & Reptile Conservation 13(2) [General Section]: 133-144 (e194).
Copyright: © 2019 Guayasamin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 7 June 2019; Accepted: 12 October 2019; Published: 10 November 2019
Introduction traits. One of the most striking traits of this genus is
its complete ventral transparency, produced by having
The glassfrog genus Hyalinobatrachium (sensu Ruiz- a transparent ventral peritoneum (Ruiz-Carranza and
Carranza and Lynch 1991, as modified by Guayasamin = Lynch 1991; Cisneros-Heredia and McDiarmid, 2007;
et al. 2009) is one of the most charismatic anuran groups § Guayasamin et al. 2009). Males of all species in this
because of its peculiar morphological and behavioral genus also exhibit extended parental care towards
Correspondence. * jmguayasamin@usfq.edu.ec
Amphib. Reptile Conserv. 133 November 2019 | Volume 13 | Number 2 | e194
A new species of Hyalinobatrachium from Ecuador
fertilized egg clutches deposited on the leaves of trees
(see Delia et al. 2017). Extended male parental care, a
derived trait that has evolved at least twice in glassfrogs,
is coupled with egg deposition on the underside of leaves
in all Hyalinobatrachium and some Centrolene species
(Ruiz-Carranza and Lynch 1991; Guayasamin et al.
2009; Delia et al. 2017; Salgado and Guayasamin 2018).
Although assigning species to Hyalinobatrachium
is straightforward, distinguishing among members
of this genus is more complicated because species of
Hyalinobatrachium tend to be remarkably similar,
both morphologically and ecologically. In recent years,
species discovery in frogs has relied heavily on molecular
and acoustic traits (Castroviejo-Fisher et al. 2009, 2011;
Kubicki et al. 2015; Guayasamin et al. 2017). Calls, in
particular, are especially useful for distinguishing among
cryptic species since they function as efficient prezygotic
mating recognition signals (Narins and Capranica 1976;
Duellman and Trueb 1994; Zakon and Wilczynski 1988:
Wilczynski and Ryan 1999; Wells 2007). As previously
demonstrated in glassfrogs, the acoustic differences
between species are often more pronounced than
morphological differences (Escalona-Sulbaran et al.
2018).
We describe a new species of Hyalinobatrachium that
is morphologically cryptic with H. anachoretus Twomey,
Delia, and Castroviejo-Fisher 2014, H. esmeralda Ruiz-
Carranza and Lynch 1998, and H. pellucidum (Lynch and
Duellman 1973). The new species, which is known from
a single locality in the Topo River basin, is differentiated
from these two species by its call and genetics.
Materials and Methods
Ethics statement. Research was conducted under
permits NoMAE-DNB-CM-2015-2017, 019-2018-IC-
FAU-DNB/MAE, and 018-2017-IC-FAU-DNB/MAE,
issued by the Ministerio del Ambiente del Ecuador. The
study was carried out in accordance with the guidelines
for use of live amphibians and reptiles in field research
(Beaupre et al. 2004), compiled by the American
Society of Ichthyologists and Herpetologists (ASIH),
the Herpetologists’ League (HL), and the Society for the
Study of Amphibians and Reptiles (SSAR).
Taxonomy and species concept. Glassfrog generic
and family names follow the taxonomy proposed by
Guayasamin et al. (2009). Species are considered
as segments of separately evolving metapopulation
lineages, following the conceptual framework developed
by Simpson (1951, 1961), Wiley (1978), and de Queiroz
(2007). Assessing whether a given population is an
independent lineage is a non-trivial task, especially
when working with closely related taxa. In such cases,
analyzing many different sets of characters provides
tools for supporting species hypotheses (Dayrat 2005; de
Queiroz 2007; Padial et al. 2009).
Morphological data. Lynch and Duellman (1973) and
Cisneros-Heredia and McDiarmid (2007) are followed
for the diagnosis and description of the new species. The
webbing formula follows Savage and Heyer (1967), as
Amphib. Reptile Conserv.
modified by Guayasamin et al. (2006). The taxonomy of
centrolenid frogs follows the proposal by Guayasamin
et al. (2009). Comparisons were made between various
Hyalinobatrachium specimens (see Appendix 1)
housed at the following collections: Instituto de Ciencia
Naturales, Universidad Nacional de Colombia, Bogota,
Colombia (ICN); University of Kansas, Museum of
Natural History, Division of Herpetology, Lawrence,
Kansas, USA (KU); Museo de Zoologia, Universidad
Tecnologica Indoamérica, Quito, Ecuador (MZUTI);
National Museum of Natural History, Smithsonian
Institution, Washington, DC, USA (USNM):; and Museo
de Zoologia, Universidad San Francisco de Quito, Quito,
Ecuador (ZSFQ). Morphological measurements were
taken with a Mitutoyo® digital caliper to the nearest
0.1 mm, as described by Guayasamin and Bonaccorso
(2004), except when noted, and are as follows: (1)
snout—vent length (SVL); (2) tibia length; (3) foot
length; (4) head length; (5) head width; (6) interorbital
distance (IOD); (7) upper eyelid width; (8) internarial
distance; (9) eye-to-snout distance; (10) eye diameter;
(11) tympanum diameter; (12) radioulna length; (13)
hand length; (14) Finger I length; (15) Finger II length
= distance from outer margin of palmar tubercle to tip
of Finger II; and (16) width of disc of Finger III. Sexual
maturity was determined by the presence of vocal slits
and calling activity in males.
Bioacoustics. Sound recordings were made with an
Olympus LS-10 Linear PCM Field Recorder and a
Sennheiser K6—ME 66 unidirectional microphone. The
calls were recorded in WAV format with a sampling rate
of 44.1 kHz/s with 16 bits/sample. Measurements and
definitions of acoustic variables follow Kohler et al.
(2017). Notes were divided into two classes—“pulsed”
and “tonal”—based upon the distinct waveforms on the
oscillogram (see Hutter and Guayasamin 2012). Pulsed
(also termed peaked) notes are defined as those with one
or more clear amplitude peaks and amplitude modulation
(i.e., visible increases and decreases in amplitude on the
oscillogram throughout the call). In contrast, tonal notes
are defined as those with no clear amplitude peak (Dautel
et al. 2011). In this study the call of Hyalinobatrachium
pellucidum (Lynch and Duellman 1973) is also described
from an individual (USNM 286708) recorded at the type
locality of the species (Rio Azuela, 0.1167°S, 77.617°W,
1,740 m, Napo province, Ecuador) by Roy McDiarmid;
the recording is deposited at the Cornell University
Macaulay Library (ML Catalogue No. 202401).
Evolutionary relationships. Mitochondrial sequences
(16S) were generated for four individuals (ZSFQ 1647—
48, 1650-51) of the new species of Hyalinobatrachium.
Extraction, amplification, and sequencing protocols were
as described in Guayasamin et al. (2008). The sequences
obtained were compared with all those available for other
species of glassfrogs (family Centrolenidae) and its sister
taxon Allophrynidae (see Austin et al. 2002; Guayasamin
et al. 2018). These sequences were downloaded from
GenBank (https://www.ncbi.nlm.nih.gov/genbank/), and
were generated mostly by Guayasamin et al. (2008),
Castroviejo-Fisher et al. (2014), and Twomey et al.
November 2019 | Volume 13 | Number 2 | e194
Guayasamin et al.
(2014), but also included data from the newly described
H. yaku Guayasamin et al. 2017 and H. muiraquitan de
Oliveira and Hernandez-Ruz 2017. Sequences were
aligned using MAFFT v.7 (Multiple Alignment Program
for Amino Acid or Nucleotide Sequences: http://mafft.
cbre.jp/alignment/software/), with the Q-INS-1 strategy.
MacClade 4.07 (Maddison and Maddison 2005) was
used to visualize the alignment (no modifications were
necessary). Maximum likelihood (ML) was run in the
IQ-TREE 1.5.5 software (Nguyen et al. 2015). The best-
fitting nucleotide substitution model was implemented
using ModelFinder within IQ- TREE (Kalyaanamoorthy et
al. 2017), which groups partitions with the same model
and similar rates, and simultaneously searches the model
and tree space. Node support was assessed via 1,000 ultra-
fast bootstrap replicates, a method that shows less bias
than other support estimates (Minh et al. 2013). Ultra-fast
bootstrapping also leads to straightforward interpretation
of the support values (e.g., support of > 95 bootstrap
should be interpreted as significant; Minh et al. 2013).
Results
Phylogenetic relationships. Based on the Bayesian
Information Criterion, the best-fit model for this dataset
was GTR+F+R5. Rate parameters were estimated as
follows: A—C: 2.690, A-—G: 9.067, A-T: 3.078, C-—G:
0.346, C—T: 23.835, and G—T: 1.000. Base frequencies
were: A = 0.346, C = 0.239, G=0.181, and T = 0.234.
The phylogeny (Fig. 1) confirms the placement of
the new species within the genus Hyalinobatrachium.
The new species, described below, is inferred as part of
a clade formed by four species that have very similar
morphologies: the new species (described below) + H.
anachoretus + H. pellucidum + H. yaku.
Species description
Hyalinobatrachium adespinosai new species
urn:lsid:zoobank.org:act:46C6CBB4-ECE3-470E-A 15C-4BB36A3301DE
Suggested English name: Adela’s Glassfrog
Suggested Spanish name: Rana de Cristal de Adela
Holotype. ZSFQ 1648 (JMG 583, Fig. 2), adult male
from riverine vegetation along the San Jacinto River
(1.3447°S, 78.1814°W; 1,795 m asl), Tungurahua
Province, Ecuador, collected by CRH, REG, and KC on
4 August 2017.
Paratypes. ZSFQ 1650-52, 1647, adult males with same
data as holotype.
Generic placement. The new species is placed in the
genus Hyalinobatrachium (Ruiz-Carranza and Lynch,
1991, as modified by Guayasamin et al. 2009) on the
basis of morphological and molecular data. The main
diagnostic phenotypic traits of Hyalinobatrachium are:
(1) ventral parietal peritoneum completely transparent;
(2) digestive tract and bulbous liver covered by
iridophores; (3) humeral spines absent; (4) white bones
Amphib. Reptile Conserv.
in life; (5) males call from the underside of leaves;
(6) females place the eggs on the underside of leaves;
and (7) males provide extended parental care. All the
aforementioned characteristics are shared by the new
species. Additionally, analyses of the mitochondrial
16S gene place the new species as a close relative of
other Hyalinobatrachium species (Fig. 1); thus, generic
placement in Hyalinobatrachium is unambiguous.
Diagnosis. Within the genus HAyalinobatrachium,
the new species is diagnosable mainly by having a
transparent pericardium. However, the new species
is morphologically cryptic with three closely related
taxa (H. anachoretus, H. pellucidum, H. esmeralda).
Based on comparisons with specimens examined (see
Appendix 1), all these species display a similar size and
color pattern (pale green dorsum with yellow dots and
a transparent venter and pericardium; red heart visible
ventrally). However, calls between species diverge
noticeably; the major difference is the structure of the
call, with two species (H. adespinosai sp. nov. and H.
anachoretus) having pulsed calls and the others having
tonal vocalizations (Fig. 3; Table 1). The call of #7.
adespinosai sp. nov. is further differentiated from that
of H. anachoretus by being longer, having more pulses
per note, and being produced at a higher rate (Table
1). Toe webbing (Toe IV) is less extensive in the new
species (2'3 IV 2°) than in H. anachoretus (1* IV 1°;
Twomey et al. 2014). Additionally, the new species and
H. anachoretus are separated by considerable distance
(airline distance = 473 km), including one of the most
important biogeographic barriers in South America, the
Marafion valley (see Duellman 1999; Winger and Bater
2015 and references therein). Uncorrected p genetic
distances for the mitochondrial gene 16S between
H. adespinosai sp. nov. and its closest relatives are
summarized in Table 2.
Characterization. The following combination of
characters is found in Hyalinobatrachium adespinosai
sp. nov.: (1) dentigerous process of the vomer lacking
teeth; (2) snout truncate in dorsal and lateral views:
(3) tympanum barely visible, hidden under skin, with
coloration similar to that of surrounding skin; (4)
dorsal skin shagreen; (5) ventral skin areolate; cloacal
ornamentation absent, paired round tubercles below vent
absent; (6) parietal peritoneum transparent; pericardium
with thin layer of iridophores (in life, a red heart is mostly
visible ventrally); liver, viscera, and testes covered
by iridophores; (7) liver bulbous; (8) humeral spines
absent; (9) hand webbing formula: I (2-3) — (2—2*) IT
(1-1*) —3'° III (2-2*) — (2—2) IV; (10) foot webbing
moderate; webbing formula: I 1— (17°-2-) I (1-1-) —
(2—2"3) IIT (1-1*) —(2*-2!%) IV 2*— (1*-1"%) V; (11)
fingers and toes with thin lateral fringes; ulnar and tarsal
folds present, but low and difficult to distinguish, with
thin layer of iridophores that extends to ventrolateral
edges of Finger IV and Toe V; (12) nuptial excrescence
present as a small pad on Finger I (Type V), prepollex
not enlarged; prepollical spine not projecting (spine not
exposed); (13) when appressed, Finger I longer than II;
(14) diameter of eye about two times wider than disc on
November 2019 | Volume 13 | Number 2 | e194
A new species of Hyalinobatrachium from Ecuador
Celsiella revocata (EU663019)
Celsiella vozmedianoi (EU663025)
H. cappellei (EU663040)
H. iaspidiense (EU663047)
H. tricolor (EU663027)
H. taylori (EU663056)
H. mondolfii_ (EU663050)
H. munozorum (EU663034)
H. pallidum (€U663052)
H. carlesvilai (KM068270)
H. carlesvilai (KM068271)
H. carlesvilai (EU663030)
H. fleischmanni (DQ283453)
H. fleischmanni (Jx564869)
H. fleischmanni (EU663045)
H. fleischmanni (EU663044)
H. tatayoi (EU663055)
H. muiraquitan (KY310571)
H. muiraquitan (KY310570)
H. kawense (EU663029)
H. duranti (EU663041)
H, ibama (EU663048)
Hyalinobatrachium sp (EU447290)
H. orientale (EU447289)
H. guairarepanense (KF534363)
H. orocostale (EU447284)
H. fragile (€U447286)
H. chirripoi (KF604294)
H. chirripoi (EU663037)
H. chirripoi (EU663038)
H. aff. colymbiphylium (kM068297)
H., aff. colymbiphyllum (KF604300)
H. aff. colymbiphyllum (FJ784471)
H. colymbiphyllum (FJ784346)
H. colymbiphyllum (FJ784475)
99
H. colymbiphyllum (FJ784527)
H. colymbiphyllum (EU663039)
H. anachoretus (KM068300)
H. anachoretus (KM068268)
H. adespinosai sp. nov. (ZSFQ-1648: MN604036)
H. adespinosai sp. nov. (ZSFQ-1651: MN604037)
H. adespinosai sp. nov. (ZSFQ-1647: MN604038)
H. adespinosai sp. nov. (ZSFQ-1650: MN604039)
H. pellucidum (GQ142065)
H. pellucidum (KM068252)
H, yaku (MF002066)
: H. yaku (MF002067)
H. aff. esmeralda (EU663036)
H. aff. esmeralda (KP149361)
H. bergeri (EU663033)
——<$$<———. Hyalinobatrachium sp (KM068298)
100
———— Hyalinobatrachium sp (KM068299)
H. vireovittatum (KF604303)
H. talamancae (EU663054)
0.02 substitutions/site
H. aff. bergeri (EU663026)
H. aureoguttatum (EU663025)
H. valerioi (EU663058)
Fig. 1. Phylogenetic relationships of Hyalinobatrachium inferred from the 16S mitochondrial gene under ML criteria. All sequences
were downloaded from GenBank, except for those of the new species. GenBank codes are listed next to each terminal. Associated
locality data is available at GenBank, as well as in Guayasamin et al. (2008), Castroviejo-Fisher et al. (2014), and Twomey et al.
(2014),
Finger III; (15) coloration in life: dorsal surfaces pale
yellowish green with small pale yellow spots and minute
gray to black melanophores; bones white; (16) coloration
in preservative: dorsal surfaces pale cream with minute
melanophores; (17) iris coloration in life: white with pale
yellow hue and numerous minute lavender spots; (18)
melanophores absent from most fingers and toes, but
present on Finger IV and Toes IV and V; (19) males call
Amphib. Reptile Conserv.
from underside of leaves; advertisement call consisting
of single note, distinctly pulsed (9-13 pulses per call),
with duration of 0.382—0.430 s, and dominant frequency
at 4,645-5,001 Hz; (20) males attend egg clutches
located on the underside of leaves overhanging streams;
clutch size of 22 embryos (n = 1); (21) SVL in adult
males 20.5—22.2 mm (n = 3), females unknown; and (22)
enameled tubercles absent from sides of head.
November 2019 | Volume 13 | Number 2 | e194
Guayasamin et al.
Fig. 2. Hyalinobatrachium adespinosai sp. nov. in life,
holotype.
Description of the holotype. ZSFQ 1648, adult male
with SVL 22.2 mm. Head wider than long (head width
38% of SVL; head length 77% of head width). Snout
truncate in dorsal and lateral views. Loreal region
flat and nearly vertical, nostrils slightly protuberant,
elliptical; internarial region concave anterodorsally;
canthus rostralis well defined. Eyes small, directed
anterolaterally, eyes about 45° relative to midline (where
Amphib. Reptile Conserv.
Amplitude (kU)
Frequency (kHz)
1:03.4 1:03.6 1:03.8
Time (m:s)
Fig. 3. Call of Hyalinobatrachium adespinosai sp. nov.,
holotype, recorded in field conditions at the type locality. Air
temperature: 18 °C.
anterior-facing eyes would be 90° relative to midline).
Tympanum annulus barely visible through the skin;
tympanic membrane differentiated and pigmented as
surrounding skin. Dentigerous processes on vomers
absent; choanae large, oval, separated widely (distance
about the same as between nostrils); tongue round, white
in preservative, anterior 4/5 attached to mouth; vocal slits
present, extending along floor of mouth lateral to tongue;
enameled glands absent from lower part of upper jaw.
Ulnar fold present, with a thin layer of iridophores, and
continuing along the external edge of Finger IV; humeral
spine absent. Relative lengths of fingers: I < II < IV <
II; finger discs rounded, about the same size as discs on
toes, disc on Finger II 54% of eye width; finger webbing
reduced between Fingers I-III, moderate between
Fingers III and IV, with formula I 3—2* II 1*—3'° I]
2 — 2 IV. Prepollex concealed; subarticular tubercles
round, faint; few small supernumerary tubercles present,
palmar tubercle round and small, thenar tubercle ovoid;
nuptial excrescences present as a small pad on external
edge of Finger I (Type V). Hind limbs slender, tibia
length 58% of SVL; tarsal fold present, with thin layer of
iridophores; discs of toes round, inner metatarsal tubercle
small; outer metatarsal tubercle round, but very difficult
to distinguish. Webbing formula of feet: I 1— 2> II 1—2'"
I 1’—2'71V—2*— 1V. In preservative, dorsal skin
peppered with small dark lavender melanophores; dorsal
skin shagreen; skin on venter areolate; cloacal opening
at level of upper thighs, cloacal ornamentation present
as a lightly enameled cloacal fold and small tubercles.
Parietal peritoneum transparent; pericardium with a very
thin layer of iridophores that, in life, exposes a red heart:
urinary bladder lacking iridophores; liver, viscera, and
testes fully covered by iridophores. Kidneys rounded,
approximately bean-shaped; liver bulbous.
Coloration in life. Dorsal surfaces apple green to
yellowish green with diffuse yellow spots and minute
gray to black melanophores. Melanophores absent
from fingers and toes, except Finger IV and Toes IV
and V. Ventrally, parietal peritoneum and pericardium
transparent, with a red heart always visible, even
November 2019 | Volume 13 | Number 2 | e194
A new species of Hyalinobatrachium from Ecuador
when a very thin layer of iridophores is present on the
S|
aS 2 = : : Erne I :
3 5 % g pericardium of some individuals. Visceral peritoneum
S < E S at ic 2 fi C of gall bladder and urinary bladder transparent; hepatic
S} ae |e & a. and visceral peritonea white; ventral vein red. Iris pale
Sm Sa a a = ellowish white, with numerous minute lavender spots.
uae, y ;
om Bones white.
So] 8 bs Dies
~ clELR 3 Of SO o eae 3 Op . : :
wo less a 4-8 2 PAS 28 Coloration in preservative. Dorsal surfaces cream
& Els oS a= a= > > H o : : i
2 SEES E ‘ap Fa = S90 8 dotted with minute dark lavender melanophores; venter
a8 | 8 is oS ae ob ar~ A § ; ; i ee
oe erg = Fw uniform cream; visceral peritoneum lacking iridophores;
x dD & - ee 2 ; i ; cme Nig
0 © pericardium with a very thin layer of iridophores. Iris
£e = T em T T silvery white with minute lavender melanophores.
BS a
acol]ees Cor) 2 =o ws wes
S$s|223. |82 22 a eat M3
—~S)EeePe PAH + "i ao oH Measurements. Measurements of the type series are
oSijegee valley S at wy H vay ; :
Sania ee 0 & S 2s 38 d & shown in Table 3.
Sr |fie [as + oe 6S BAe
23 - < i el % Le es Ete red Ae
3 5 Variation. Variation in hand webbing is as follows: I
nN —| aj
26 Zs Poe Bee (2-3) — (2-2") LICL IR) —3"3 TI] (2-2") — (2-2) IV.
vQ|35 Z Steg dente Lie Foot webbing variation is as follows: I 1— (17°-2-) II
SY a n = =
SS \E2 ae RE (1-1-) —(2—2!) IIT (1-1*) —(2*-2!) IV 2*— (1*-1'*)
gs V.
for}
ae o™~ o™~
a2] = S a = lows ya
zselea On - = ae am Vocalizations (Fig. 3). The description is based on
ao Oo é = wy ia = on oH oo 4H H = : ih
ee ee T 2% A 7S silts. it. recordings from nine individuals (Codes LBE-C: 048—
pate | ae = Ga Pe say 0 he call of Hyalinobatrachium adespinosai
o/s ole a uv WU 57). The call of Hyalinobatrachium adespinosai sp.
al ae we cs re] by nov. has a striking resemblance to the chirp of a cricket,
See and was often confused for one in the field. Each call is
8/3 +H = ¥ = composed of a single and high-pitched pulsed note, and
on he Oo : Se ‘
3 = 12 mee . 4 aus + has a duration of 0.38-0.44 s (xX = 0.38 + 0.017). Time
n = so N | oe Oe . —_
as lg ajo |S D TIS f between calls varied from 2.0-11.0 s (X = 4.58 + 2.3).
G = & — ae ef The fundamental frequency, the same as the dominant
Seni, frequency, is at 4,645—5,203 Hz (X = 4,855 + 152). There
= | , (is
Sal’ is no frequency modulation. The first harmonic is at
Ow S : *
24 = 3 3 = = = 9,336—9,754 Hz and the second harmonic is at 14,159-—
a n nA fon i= S
Rep le = = e e 2 14.444 Hz
_ Oo @ & & am ome cH > ;
Fels
s = Ecology. All individuals of the new species were found
S 5/5 on the underside of leaves of riverine vegetation along the
gS eR 2. " ' * ' :
Ss e/8 3 x - ¥. = = San Jacinto River. The section of river was fast-flowing
oe) =) ae ‘ : A
S&|5 and had visible rapids. Although the population is locally
Ss + 7
8 8 abundant (as heard from numerous advertisement calls
eS Sack .
ron le oe eats a mH es uh individuals are very difficult to observe because they are
SS(EPFESISRS FS SRF S8S Sag lly found at th level (4-16 mab d
Aes es 2.8 Siok S SAY cst cs8a usually found at the canopy level ( m above groun
oS /Sts ely Cs a eres lcs ye ; . :
5 §/seess|S Le & Rupe eS NO? level). The type series consists of males exclusively; they
a. RS Crm vi a a were calling in the months of July and August. One male
3% <a (ZSFQ 1648) was apparently guarding an egg clutch
a containing 22 embryos; both the adult male and the egg
Csletss IE Si = 2 =
SBlEsts |& = = = S clutch were on the same leaf most of the time, but the
Ooh ler ay ‘ male also moved to nearby leaves (Fig. 4).
o.5 A
aes
ae) eae :
Ss 3 g 3 « : 30 os g& Distribution. Hyalinobatrachium adespinosai_ sp.
Ss a 4 6 . ‘ :
ane le § Ex sao sg, BEI § nov. is only known from the type locality: San Jacinto
[a0] — N a) . A i) :
he = eas soc E 88s ee%, FS River (1.3447°S, 78.1814°W; 1,795 m asl), Tungurahua
+2 2 Ge | 2s San Ct en : ‘
on be Ros “So seat BES kg Province, Ecuador (Fig. 5).
& 16 gee poo, Cree SN Ss 3§
ay eet eee EES ASE
== ae i . “es AS Evolutionary relationships. The phylogenetic
28 analyses recover Hyalinobatrachium adespinosai sp.
= = ¢. nov. haplotypes as sister to haplotypes sampled from
pan ae i in
5 8 5 s . S H. anachoretus and nested within other members of
> S S Ss = ;
= 8 & s S iS a monophyletic clade comprised of all other sampled
n 7.) : s : F - :
2 s z 8. S 5 3 $ species of Hyalinobatrachium (Fig. 1). The most closely
iS 3 & a ~ ~ = ~ related species to H. adespinosai sp. nov. share several
Amphib. Reptile Conserv. 138 November 2019 | Volume 13 | Number 2 | e194
Guayasamin et al.
f
\ f
~~ .
- >
< \ >
ag ay
egg clutch; other males were observed on the same leaf as the egg clutch. (B) Close-up of the egg clutch. (C) Spider predation on
an unattended egg clutch.
morphological traits, including a red heart exposed
ventrally (H. adespinosai + H. anachoretus + H.
pellucidum + H. yaku).
Etymology. The specific epithet adespinosai honors
Adela Espinosa, an Ecuadorian conservationist and
board member of the Jocotoco Foundation (http://
www.jocotoco.org). Adela’s work has focused on the
conservation of species and ecosystems. The new
glassfrog described here is found only within the limits
of a natural reserve owned by Adela and her husband,
Antonio Paez. We are delighted to recognize Adela’s
devotion to nature with this marvelous species.
Conservation status. Available information is
insufficient to fully assess the conservation status of
Hyalinobatrachium adespinosai sp. nov. Therefore,
following IUCN criteria, this species is considered as
Data Deficient. The herpetological museums that house
specimens collected near the type locality (Topo basin)
were consulted, but there were no additional specimens
of the new species. Although this might suggest a
conservation category other than Data Deficient, we
actually prefer to maintain this status because the new
Species 1s very difficult to find (1.e., a canopy specialist).
Therefore, in this case, absence in nearby localities
where herpetological surveys have been carried out does
not necessarily indicate a true absence of the species.
Discussion
Morphological stasis is expected in species under similar
ecological conditions, whereas traits associated with
social signaling tend to evolve more rapidly (Winger
and Bater 2015; Arnegard et al. 2010; Safran et al.
2013; Escalona-Sulbaran et al. 2018). Species in the
glassfrog genus Hyalinobatrachium exhibit a striking
morphological homogeneity (see Ruiz-Carranza and
Table 2. Genetic distances (uncorrected p matrix for 16S, 813 base pairs) between Hyalinobatrachium adespinosai sp. nov. and
closely related species.
H. adespinosai H. anachoretus
H. adespinosai 0.000-0.001
HZ. anachoretus 0.010-0.011 0.000
H.. esmeralda 0.0254—0.0272 0.0272
H. pellucidum 0.032-0.034 0.029-0.037
HA. yaku 0.036—0.037 0.033—0.041
Amphib. Reptile Conserv. 139
H. esmeralda H. pellucidum HA. yaku
0.000
0.034—0.040 0.007—0.009
0.038—0.040 0.025—0.030 0.000—0.001
November 2019 | Volume 13 | Number 2 | e194
A new species of Hyalinobatrachium from Ecuador
ok ft A -76°
Colombia
Fig. 5. Distribution of Hyalinobatrachium adespinosai sp. nov. in Ecuador.
Lynch 1998; Guayasamin et al. 2009; Castroviejo-Fisher
et al. 2011), perhaps because of the constraints associated
not only with their similar ecology, but also with their
derived reproductive strategy (prolonged parental care
on the underside of leaves). The obvious consequence is
that traditional morphological trait-based criteria provide
an underestimation of the true biological diversity of the
genus. In contrast, call traits in centrolenids have shown
more variation that morphology (Escalona-Sulbaran et
al. 2018). Acoustic signals can diverge because of the
effects of multiple mechanisms, including drift (e.,
isolation-by-distance), natural selection (1.e., adaptation
to local ecological conditions, reinforcement, character
displacement), and/or sexual selection (1.e., sensory
exploitation, divergent female choice; reviewed by
Wilczynski and Ryan 1999; Wells 2007; Prum 2017;
Kohler et al. 2017). However, this study represents
another example of how vocalizations can be extremely
useful for species discovery.
Given the lack of information for Hyalinobatrachium
adespinosai sp. nov., we consider the species as Data
Deficient, following the IUCN criteria. The species is
Amphib. Reptile Conserv.
locally abundant at the type locality and as currently
known has a restricted distribution. However, given that
the species is usually found at the canopy level, it is
extremely difficult to locate individuals of this species,
So we cannot infer its true distribution based solely on the
lack of prior collection.
Establishing clear biogeographic patterns in
groups where new species are often being described
is challenging. However, Hyalinobatrachium species
are generally found in the lowlands while Centrolene
and Nymphargus species are predominantly Andean
(Guayasamin et al. 2009; Hutter et al. 2017). In contrast
to these general patterns, the clade formed by H.
adespinosai sp. nov. + H. anachoretus + H. pellucidum
+ H. yaku + H. esmeralda is mostly found on the
Amazonian slopes of the Andes (except H. yaku). Since
tropical species tend to have narrow thermal niches (Shah
et al. 2017, Polato et al. 2018), the linearity of the Andean
mountain range might promote speciation by reducing
contact and gene flow among parapatric populations (see
Fig. 6), as suggested by Graves (1988). Similar patterns
(i.e., closely related species along the same slope of
November 2019 | Volume 13 | Number 2 | e194
Guayasamin et al.
Lineary of the Andes:
Loss of connectivity because of random local extinction
Lineary of the Andes:
Loss of connectivity because of valleys (ecological barriers)
3 Species
Species C
eee SSS
Fig. 6. Schematic graph illustrating how the linearity of the Andes facilitates the speciation process.
the Andes) have also been observed in other glassfrogs
(e.g., Nymphargus; Guayasamin et al. 2019) and birds
(Bonaccorso 2009; Benham et al. 2015; Cadena et al.
Table 3. Meristic variation of Hyalinobatrachium adespinosai
sp. nov. (in mm).
2019). ZSFQ ZSFQ ZSFQ
1647 1651 1647
Acknowledgments.—Two reviewers (Alejandro Arteaga (holotype)
and an anonymous reviewer) provided comments that ae Male Male Rigie
greatly improved this article. Research permits were
issued by the Ministerio de Ambiente del Ecuador SVL 22.2 20.7 20.5
(MAE-DNB-CM-2015-0017, 019-2018-IC-FAU-DNB/ Femur 12.8 12.0 12.1
USNM for providing access to specimens housed at their
collections. This study was supported by the Universidad Foot m0 sue 10P
San Francisco de Quito (Equipamiento del Laboratorio Head length 6.5 6.4 6.2
de Biologia Evolutiva, project ID 5467; Ranas de Cristal: Head width 84 rg PO
Taxonomia, Evolucion y Conservacion, project ID 5466), IOD 28 25 6
and the Programa Inédita from Secretaria de Educacion
Superior, Ciencia, Tecnologia e Innovacion (Project: Upper eyelid 1.6 1.4 1.6
Respuestas a la crisis de biodiversidad: la descripcion Internarinal 1.8 1.7 1.7
de especies como herramienta de conservacion). Finally, distance
our most warm thanks to Walt and Linda Jennings for Eye diameter 16 23 23
supporting the wonderful conservation efforts in Ecuador. EeePONt 39 28 3.0
, . distance
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A new species of Hyalinobatrachium from Ecuador
Appendix 1. Examined Specimens
Hyalinobatrachium esmeralda: Colombia: Boyaca Department: Municipio de Pajarito, Inspeccién Policia Corinto,
finca'El Descanso’, quebrada'La Limonita', 1,600—1,650 m, ICN 9592-94, 9596, 9602-03 (type series of H. esmeralda).
Hyalinobatrachium pellucidum: Ecuador: Morona Santiago Province: Nueva Alianza, Finca Santa Catalina
(78.1335°W, 2.100°S; 1,305 m), Limite del Parque Nacional Sangay, MEPN 14706. Quebrada del Rio Napinaza
(78.4070°W, 2.9266°S, 1,100 m), QCAZ 42000; km 6.6 on the Limon-Macas road (ca. 2.92816°S, 78.344°W; 1,013
m), QCAZ 29438; 6 km N of Limon, QCAZ 25950. Sucumbios Province: Rio Azuela (0.1167°S, 77.6167°W, 1,740
m), Quito-Lago Agrio road; KU 164691 (holotype), USNM 286708—10; Rio Reventador, USNM 286711-—12. Zamora
Chinchipe Province: Cordillera del Condor, Miazi Alto (4.25044°S, 78.61356°W; 1,282 m), QCAZ 41560-61, 41648.
Hyalinobatrachium munozorum: Ecuador: Sucumbios Province: Santa Cecilia (00°03'N, 76°58'W; 340 m), KU 118054
(holotype), 105251, 123225, 150620 (paratypes), 152488—-89, 155493-96, 175504. Orellana Province: Tiputini
Biodiversity Station, ZSFQ DFCH-USFQ D105. Colombia: Meta Department: Meta, ICN 5031-34, 39503. Amazonas
Department: Leticia, ICN (field number JMR 4119).
Hyalinobatrachium yaku: Ecuador: Pastaza Province: stream affluent of the Kallana river (1.4696°S, 77.2784°W;
325 m), MZUTI 5001 (holotype), 5002 (paratype). Orellana Province: Timburi-Cocha Research Station (0.4800°S,
77.2829°W; 300 m) near San José de Payamino, QCAZ 55628, QCAZ 53352, 53354, 56664. Napo Province: Ahuano
(1.0632°S, 77.5265°W; 360 m), ZSFQ 02322.
Juan M. Guayasamin is a professor at Universidad San Francisco de Quito, Ecuador, and
codirector of the Laboratory of Evolutionary Biology. Juan obtained his Master’s and Ph.D.
degrees in ecology and evolutionary biology from the University of Kansas (Lawrence,
Kansas, USA) under the supervision of Dr. Linda Trueb. He is member of the Ecuadorian
Academy of Sciences and has published more than 80 scientific papers on evolution,
systematics, biogeography, and conservation of Neotropical animals, mainly amphibians.
Jose Vieira is a field biologist, wildlife photographer, and tour leader from Venezuela. From
a young age, Jose became passionate about nature, particularly amphibians and reptiles. This
passion led him to participate in countless field expeditions in his native country, and from
them Jose has contributed many herpetological specimens to the Museo de Historia Natural
La Salle. Currently, his contributions to science continue in Ecuador with the rediscovery of
the critically endangered Ate/opus bomolochos and A. nepiozomus, and his expeditions to
remote areas of the country to work on various herpetological projects of Tropical Herping
and Universidad San Francisco de Quito.
Richard E. Glor is a Professor in the Department of Ecology and Evolutionary Biology,
and a Curator in the Biodiversity Institute, at the University of Kansas (Lawrence, Kansas,
USA). Richard studies the evolution of species diversity, primarily through work on West
Indian anole lizards. He received his Bachelor’s degree from Cornell University (Ithaca,
New York, USA), his doctorate in Ecology and Evolutionary Biology from Washington
University (St. Louis, Missouri, USA), and conducted postdoctoral research in the Center
for Population Biology at University of California, Davis.
Carl R. Hutter recently obtained his Ph.D. from the University of Kansas (Lawrence,
Kansas, USA). Carl is interested in amphibians and has done field research in Madagascar and
Ecuador. He is currently focusing on the evolution of advertisement calls in frogs, especially
seeking to understand how environmental influences lead to the evolution of distinct calls.
Carl is also interested in the phylogenomics of frogs, and is working to understand anuran
phylogenetic relationships at the Order level, as well as within several families.
Amphib. Reptile Conserv. 144 November 2019 | Volume 13 | Number 2 | e194
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 145-151 (e196).
New records and distribution extension of the rare glassfrog
Hyalinobatrachium chirripoi (Anura: Centrolenidae)
throughout the Choco-Magdalena region in Colombia
1.2.3.*Angela M. Mendoza-Henao, ‘Roberto Marquez, °Claudia Molina-Zuluaga,
SDaniel Mejia-Vargas, and °Pablo Palacios-Rodriguez
‘Departamento de Zoologia, Instituto de Biologia, Universidad Nacional Autonoma de México, PO 70-153, 04510 Mexico City, MEXICO *Posgrado
en Ciencias Biologicas, Universidad Nacional Autonoma de México, PO 70-153, C.P. 04510, Mexico City, MEXICO *Grupo de Investigacion en
Ecologia y Conservacion Neotropical, 760046, Cali, COLOMBIA *Department of Ecology and Evolution, University of Chicago. 1101 East 57th
St. Chicago, Illinois 60637, USA °Grupo Herpetolégico de Antioquia, Instituto de Biologia, Universidad de Antioquia, A. A. 1226, Medellin,
COLOMBIA °Department of Biological Sciences, Universidad de los Andes, A.A. 4976, Bogota, COLOMBIA
Keywords. Amphibia, Andes Mountains, DNA barcoding, South America, rainforest, range extension
Citation: Mendoza-Henao AM, Marquez R, Molina-Zuluaga C, Mejia-Vargas D, Palacios-Rodriguez P. 2019. New records and distribution extension
of the rare glassfrog Hyalinobatrachium chirripoi (Anura: Centrolenidae) throughout the Chocé-Magdalena region in Colombia. Amphibian & Reptile
Conservation 13(2) [General Section]: 145-151 (e196).
Copyright: © 2019 Mendoza-Henao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 9 January 2019; Accepted: 16 August 2019; Published: 16 December 2019
Hyalinobatrachium is the most diverse glassfrog genus
(family Centrolenidae) with 32 species described to
date, ranging from Mexico to Argentina (Guayasamin
et al. 2009; Frost 2019). Given the low levels of
morphological differentiation within this genus, species
identification is sometimes difficult, and requires the
use of alternative sources of evidence such as molecular
phylogenetics and DNA barcoding (Castroviejo-Fisher
et al. 2009). Hyalinobatrachium chirripoi (Taylor 1958)
is a seldom observed species found in forests under 600
m elevation from Honduras, along the Choco-Darien
to the Esmeraldas Province in north Ecuador (Kubicki
2007; Guayasamin et al. 2016). Here new records of
H. chirripoi are reported which extend the distribution
of this species into the Andean foothills of the central
Choco and, for the first time, into the Magdalena Valley
of Colombia. An overview of the known distribution
H. chirripoi 1s presented, including previous museum
records and the new data.
Specimens examined. One individual was collected in
2010 at Vereda El Porton, in San Francisco, Antioquia,
Colombia (5.9015, -74.96925, 589 m asl; Fig. 1), in the
Magdalena River drainage. The individual was found
at night, calling on the underside of a Heliconia leaf
overhanging a small stream in a secondary forest, and
was euthanized with an overdose of 2% Roxicaine and
fixed in 10% formalin. A liver sample was preserved in
99% ethanol. The specimen was deposited in the Museo
de Herpetologia, Universidad de Antioquia, Colombia
Correspondence. * am.mendozah@gmail.com
Amphib. Reptile Conserv.
(voucher MHUA-A 06650; originally misidentified
as H. fleischmanni). In 2016, two other individuals
were collected during nocturnal surveys performed
at 20 km SW of Condoto, Choco, Colombia, on the
western versant of the Cordillera Occidental (5.02078,
-76.51633, 423 m asl; Fig. 1A). They were found calling
from the upper side of leaves in a tree hanging above a
small river (Fig. 1B). They were captured and euthanized
with an overdose of topical lidocaine hydrochloride
(Xylocaine). Muscle samples were stored in 100%
ethanol. Specimens were then fixed with 100% ethanol
and deposited in the herpetology collection of the Natural
History Museum at Universidad de los Andes, Colombia
(vouchers ANDES-A3738 and ANDES-A3739). Other
individuals at the same locality were observed on leaves
and fronds of Araceae, Musaceae (Heliconia), and ferns
(Polypodiaceae), perched ~3—8 m off the ground. Both
localities (Vereda El Porton at the Magdalena River
drainage, and 20 km SW of Condoto in the Choco) are
classified as tropical wet forest biome (bh-T, Holdridge
1964).
Morphological and molecular identification. These
samples were identified as H. chirripoi based on light
dorsal spots, significant webbing between Fingers II and
II, clear parietal peritoneum, bare heart condition (.e.,
iridophores covering all visceral peritonea except for the
urinary bladder and pericardium), tympanum visible,
and a truncate snout in sagittal view (Taylor 1958; Ruiz-
Carranza and Lynch 1998; Savage 2002, Fig. 2). To
December 2019 | Volume 13 | Number 2 | e196
Hyalinobatrachium chirripoi in Colombia
0 125 250 375 500
Museum records
N
\ re Ki
@
& New Records
Fig. 1. (A) Localities of museum specimens (black dots) and new records (red dots) for Hyalinobatrachium chirripoi. Coordinates
for specimen IAVH-A-4311 (gray dot) were approximated to the urban area of Rio Guapi, Cauca, since precise coordinates of the
collection site were lacking. (B) Habitat where the ANDES-A individuals were encountered.
further corroborate morphological diagnoses, mtDNA
barcoding was used. DNA was extracted following
Ivanova et al. (2006) for specimens ANDES-A3738
and ANDES-A3739, or using the Thermo Scientific
DNA extraction kit for specimen MHUA-A 06650.
Amplification of 16S (567 bp) and COI (609 bp) loci
was as described by Guayasamin et al. (2008), and
Mendoza et al. (2016; primers from Meyer et al. 2005),
respectively. Purified products were Sanger-sequenced
in both directions. Sequences obtained are deposited in
GenBank under accession numbers MH129045—49.
Sequences of both genes were blasted against the
GenBank non-redundant database using megaBLAST.
COI sequences were also used as input for the BOLD
DNA barcoding system (Ratnasingham and Hebert 2007).
In addition, Kimura-two-parameter (K2P; Kimura 1980)
pairwise distances between sequences of closely related
Hyalinobatrachium species available in GenBank (Table
1) were calculated using MEGA7 (Kumar et al. 2016) and
maximum likelihood and Bayesian mtDNA genealogies
were built with RAxML v.8.2.10 (Stamatakis 2006,
2014), and MrBayes 3.2.2 (Ronquist and Huelsenbeck
2003, Ronquist et al. 2012), respectively.
Maximum likelihood searches used the rapid _hill-
Amphib. Reptile Conserv.
climbing algorithm and 10,000 rapid bootstrap pseudo-
replicates to assess nodal support. In MrBayes two
independent 2,000,000 generation analyses were run,
sampling every 1,000 generations, and with 20% burn-in.
The best models for molecular evolution for the 16S and
for each codon position of the COI gene were selected
using PartitionFinder 2 (Lanfear et al. 2016).
Mitochondrial sequences unambiguously confirmed
the identity of the specimens as H. chirripoi. All
BLAST searches against GenBank returned H. chirripoi
sequences as the top hit, with 99% identity and e-values of
zero. Online BOLD identification searches matched the
COI sequences to H. chirripoi with 99.3—99.5% identity.
On the other hand, H. fleischmanni sequences matched
the query sequences with 83.8% similarity (BOLD) and
83.6% identity (GenBank). Maximum likelihood and
Bayesian trees corroborated these results, with the query
sequences nested within a well-supported clade that
includes all the other H. chirripoi (Fig. 3). Finally, K2P
distances among H. chirripoi samples averaged 0.006
(range = 0.002-0.009) for 16S and 0.027 (O—0.039) for
COI, while the mean distance with H. colymbiphyllum,
its sister species, was 0.021 (0.018—0.024) for 16S and
0.081 (0.059-0.093) for COI.
December 2019 | Volume 13 | Number 2 | e196
Mendoza-Henao et al.
Fig. 2. Dorsal (a) and ventral (b) view of live specimen from Chocé-Darien (ANDES-A-3738). Dorsal view (c) of specimen collected
a =
in Madgalena basin (MHUA-A-6650). Details of hand webbing of specimens collected in Choc6-Darien (d) and Madgalena basin (e).
Distribution and conservation implications. The
records of H. chirripoi since its rediscovery by Kubicki
(2004) are very scarce. In Colombia there have been very
few isolated records of the species (Hayes and Starret
1980; Romero-Martinez et al. 2008; Ruiz-Carranza and
Lynch 1998). Most previous records for the species in
Colombia are restricted to the Northwest Choco-Darien
region close to Panama, in Nuqui (MHUA-A 5150-53),
and in Bahia Solano (ICN 40270-314) (Fig. 1). One
additional specimen was collected in 1987 further south,
near Rio Guapi, Cauca (specimen [AVH-Am-4311) with
no georeferenced locality (gray circle in Fig. 1) and the
southernmost specimens were collected from Esmeraldas
Provinces in Ecuador (QCAZ-A 48271, QCAZ-A 66603,
Guayasamin et al. 2016). The new records reported
here fill the gap in the Choco-Darien between the Bahia
Solano and Rio Guapi records, extending the distribution
of this species 70 km into the Chocoan mainland and into
the foothills of the Western Andes (400 m asl).
These records also extend the distribution of H.
chirripoi into the Magdalena basin, across the Andes
from all previous records of this species. Previously, the
closest record of H. chirripoi to the Magdalena basin
was from the Cerro Murrucucu in Tierralta, Cordoba,
Amphib. Reptile Conserv.
within the Parque Nacional Natural Paramillo (ICN
39129-30), an intermediate zone between Choco-Darien
rainforests and Magdalena basin. This region is included
in the Sinu-San Jorge District, characterized by a biota
with common elements, including several amphibian
species of the Chocoan, Amazonian, and Magdalenian
regions (Henao-Sarmiento et al. 2008; Hernandez-
Camacho et al. 1992a; Marquez et al. 2017; Romero-
Martinez et al. 2008; Vasquez and Serrano 2009), and
is considered as a transition zone between the Choco-
Darien, Caribbean, and Magdalena bioregions (Romero-
Martinez et al. 2008). Congruently, the Magdalena basin
record reported here lies within the Nechi District, for
which the biological elements have affinity with those
from the upper Sint and high San Jorge drainages, as
well as the Choco-Darien region (Hernandez-Camacho
étal. 9926).
With these new records of H. chirripoi, the
Magdalena basin and Choco-Darién regions in Colombia
share a total of five species of the genus (including H.
fleischmanni, H. colymbiphyllum, H. aureoguttatum, and
H. valerioi). Hyalinobatrachium aureoguttatum and H.
valerioi are easily differentiable by the dorsal coloration
(large yellow round spots on a green background), but
147 December 2019 | Volume 13 | Number 2 | e196
Hyalinobatrachium chirripoi in Colombia
H. bergeri MHNC 5676
H. pellucidum MNCN 45955
H. aff. pellucidum MAR 2195
1/100
H. esmeralda LSB 384
1/100
H. anachoretus CORBIDI 10462
1/100
H. anachoretus CORBIDI 10472
0.6/10 1/40
0.86/50
1/100
0.02
H. colymbiphyllum KRL 0756
H. colymbiphyllum CH 6822
1/100
H. colymbiphyllum CH 6829
ita H. chirripoi CRAC1005 CR
H. chirripoi CRAC1013 CR
H. chirripoi UCR 17424 CR
D7 /80
H. chirripoi USNM 538586 HN
H. chirripoi AJC 1841 PA
0.8/100 H. chirripoi MHUA A 6650 CO
H. chirripoi ANDES A3738 CO
0.9
-H. chirripot ANDES A3739 CO
Fig. 3. Phylogenetic positions of three Hyalinobatrachium chirripoi samples from Choco and Antioquia, Colombia, in a Bayesian
mtDNA tree inferred from 16S rRNA and COI sequences. The chosen models of evolution using Partition finder were: 16S: GTR+I,
COI position 1: GTR+I, position 2: SYM+G, and position 3: F81+I. Samples in bold are from this study, while the others are
from GenBank. Posterior probability and bootstrap support values (from a maximum likelihood analysis) are indicated in front
of the corresponding node as PP/Bootstrap. Two letter country codes provided for H. chirripoi samples follow the International
Organization for Standardization: CO = Colombia, PA = Panama, HN=Honduras, CR = Costa Rica.
misidentification is common for the other three species
(Kubicki 2004). The most relevant external feature for
differentiating H. chirripoi is the extensive webbing
between Fingers II-III] (H. colymbiphyllum and_ H.
fleischmanni have little webbing between Fingers
II-III); additionally H. fleischmanni has _iridophores
covering the pericardium, while H. chirripoi and H.
colymbiphyllum \ack iridiophores in the pericardial
peritonea (Savage 2002; Starret and Savage 1973, but
check Cisneros-Heredia and McDiarmid 2007). After a
detailed revision of the H. fleischmanni specimens for the
Magdalena basin stored in the Museo de Herpetologia
of Universidad de Antioquia, no additional misidentified
H. chirripoi were found. However, this work highlights
the importance of carefully inspecting museum
specimens of Hyalinobatrachium (and other taxa with
Amphib. Reptile Conserv.
low morphological differentiation between species)
when using such specimens for biogeographic and
conservation work, in order to avoid errors associated
with misidentification.
A shortage of information still remains on the
amphibian diversity in Choco-Darien rainforest and
Magdalena basin, both of which are increasingly
threatened by human activities such as mining, habitat
loss, fragmentation, and other forms of landscape
transformation (Etter and van Wyngaarden 2000; Rangel
2004). Indeed, according to the IUCN Red List, certain
populations of H. chirripoi in Panama and Colombia are
threatened by habitat loss, due to increasing agricultural
activity and logging (Solis et al. 2008). The new records
presented here provide additional information about
the distribution of this rare species, and highlight the
December 2019 | Volume 13 | Number 2 | e196
Mendoza-Henao et al.
Table 1. Sequences for mitochondrial regions 16S and COI of
Hyalinobatrachium chirripoi and related species used in this
study.
Species Voucher 16S COI
H. chirripoi ANDES-A3738 MH129045 MH129047
H. chirripoi ANDES-A3739 MH129046 MH129048
H. chirripoi MHUA-A-6640 MH129049 NA
H. chirripoi UCR 17424 EU663037 NA
H. chirripoi USNM 538586 EU663038 NA
H. chirripoi AJC 1841 KF604299 KF604294
H. chirripoi CRAC1005 NA KJ703 104
H. chirripoi CRACI013 NA KJ703105
H. bergeri MHNC 5676 EU663033 NA
H. pellucidum MNCN 45955 KM068262 NA
H. esmeralda LSB 384 KP149361 KP149161
H. colymbiphyllum KRL 0756 FJ784359 NA
H. colymbiphyllum CH 6829 KR863254 KR862999
H. colymbiphyllum CH 6822 KR863256 KR863001
H. anachoretus CORBIDI 10462 KM068268 NA
H. anachoretus CORBIDI 10472 KM068300 NA
H. aff. pellucidum MAR-2195 KM068296 NA
importance of using an integrative taxonomic approach
at the junction between these two bioregions in terms
of biodiversity conservation, as well as the need for
continued documentation of their biological richness.
Acknowledgements.—This research _is___ partially
supported by UNAM PAPIIT: 203617, by National
Geographic Society Young Explorer’s grant (No. 9786-
15), and by the Rufford Foundation (Rufford Small
Grant reference 18423-1). AMM was supported by
a scholarship from Consejo Nacional de Ciencia y
Tecnologia (CONACyT, Mexico), through Posgrado de
Ciencias Biologicas, Universidad Nacional Autonoma de
Mexico (UNAM). Collections were authorized by permit
No. IBD0359-Res 1117-2014 from the Colombian
Environmental Licensing Authority (ANLA). Fieldwork
in the Magdalena was part of the wildlife characterization
inside the Environmental Impact Assessment (EIA) of
the Samana Norte Hydroelectric exploitation project,
funded by Integral Ingenieria de Consulta S.A and
the specimen collection was conducted under permit
No. 134-0074 granted by the Corporacién Autonoma
Regional de las Cuencas de los rios Negro y Nare -
CORNARE. We thank Mailyn A. Gonzalez and Eduardo
Tovar Luque from Instituto Alexander von Humboldt
(Bogota, Colombia) for access to laboratory facilities;
Andrew J. Crawford, Yiselle Cano, and Luis Alberto
Farfan (Universidad de los Andes, Colombia) facilitated
specimen deposition and access at the ANDES museum;
Mauricio Rivera-Correa provided the images of the
hands of the specimen from Magdalena basin; and Henry
Amphib. Reptile Conserv.
Agudelo-Zamora provided the images from specimens
deposited at Instituto de Ciencias Naturales, Facultad
de Ciencias, Universidad Nacional de Colombia. We
thank Celsa Sefiaris and Jesse Delia for their invaluable
comments to earlier versions of this manuscript, and
Juan M. Daza (Universidad de Antioquia, Colombia)
for access to Museo de Herpetologia Universidad de
Antioquia (MHUA) and his invaluable support in the
development of this manuscript.
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December 2019 | Volume 13 | Number 2 | e196
Amphib. Reptile Conserv.
Mendoza-Henao et al.
Angela M. Mendoza-Henao is a biologist from Universidad del Valle (Colombia) with an M.S.
in Biological Sciences, and a current Ph.D. student at the Universidad Nacional Autonoma de
México (UNAM). Angela’s work has focused mainly in the application of molecular tools for
solving questions in ecology and conservation, with an emphasis on terrestrial vertebrates, mainly
neotropical amphibians.
Roberto Marquez is a Ph.D. candidate in Ecology and Evolution at the University of Chicago
(Chicago, Illinois, USA). Roberto’s research is mostly focused on evolutionary genetics,
systematics, development, and behavior of Dendrobatid poison frogs. He earned B.Sc. and M.Sc.
degrees from Universidad de los Andes in Bogota, Colombia.
Claudia Molina-Zuluaga is a biologist from Universidad de Antioquia (Colombia), with an MLS. in
Biological Science from Universidad Nacional Autonoma de México (UNAM). Claudia’s research
is mostly focused on the population ecology of amphibians and reptiles, using a demographic
methods approach to population dynamics in order to establish long-term trends and conservation
status.
Daniel Mejia-Vargas is a biologist doing independent research on the systematics, biogeography,
and behavior of poison frogs. Daniel is also involved in ethnobiology research and studies diversity
in plants, fishes, amphibians, and birds.
Pablo Palacios-Rodriguez is a biologist working on his Ph.D. in Biological Sciences at Universidad
de los Andes (Colombia). Pablo is interested in the evolution of toxicity, the discovery of new
species, and the physiology of the personality of frogs.
151 December 2019 | Volume 13 | Number 2 | e196
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 152-159 (e198).
Natural history notes on three sympatric frogs, Amolops
formosus (Gunther 1875), Nanorana liebigii (Gunther 1860),
and Ombrana sikimensis (Jerdon 1870), from Manaslu
Conservation Area, Nepal
'*Biraj Shrestha and 7Min Bahadur Gurung
'SAVE THE FROGS!, 1968 South Coast Hwy Suite 622, Laguna Beach, California 92651, USA *Small Mammals Conservation and Research
Foundation, Lalitpur, NEPAL
Abstract.—Three stream dwelling mountain frogs, Amolops formosus, Nanorana liebigii, and Ombrana
sikimensis are sympatric species, native to Asia and distributed much across Nepal. Here, a brief natural
history account of the three species is provided that enhances the existing knowledge of these understudied
frogs. Altogether 21 adults (eight Amolops formosus, six Nanorana liebigii, and seven Ombrana sikimensis)
were collected from the streams of Sirdibas, Chumchet, and Bihi villages in April and May 2016 and in March
2017. Since the survey time coincided with breeding season, egg clutches and tadpoles of Nanorana liebigii
were observed. Basic morphometric features of the adults (snout-vent length, head length, head width,
femur length, and tibia length) and tadpoles (total length, body length, body width, and tail muscle width)
were measured with a Mitutoyo digital Vernier caliper to the nearest 0.1 mm. Environmental parameters of
the habitat were also noted, including air temperature, water temperature, relative humidity, and pH of the
water body. A review of the conservation status of these sympatric frogs highlights the threats they face from
unchecked harvesting in Manaslu and across the entire mountain villages of Nepal. Other potential threats
include declining stream habitats through water use management decisions such as dams and diversions,
pollution, and forest degradation. The field observation data collected will help to fill in the knowledge gaps for
these species, in order to prioritize conservation action and aid future research.
Keywords. Amphibia, Anura, Asia, habitat degradation, morphometrics, threats
Citation: Shrestha B, Gurung MB. 2019. Natural history notes on three sympatric frogs, Amolops formosus (Gunther 1875), Nanorana liebigii
(Gunther 1860), and Ombrana sikimensis (Jerdon 1870), from Manaslu Conservation Area, Nepal. Amphibian & Reptile Conservation 13(2) [General
Section]: 152-159 (e198).
Copyright: © 2019 Shrestha and Gurung. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 16 August 2018; Accepted: 25 July 2019; Published: 11 November 2019
Introduction
Amolops formosus, Nanorana liebigii, and Ombrana
sikimensis are sympatric species that are largely dependent
upon mountain brooks and associated riparian habitats
characterized by coniferous or oak forests (Schleich and
Kastle 2002). They are native to Asia, found across many
of the mountains of Nepal, and also recorded in India,
China, Bangladesh, and Bhutan (Bordoloi et al. 2004;
Liang et al. 2004). In Nepal, they are distributed within
an altitudinal range of 1,190-3,360 m asl (Schleich
and K4astle 2002). All three species were previously
placed in the genus Rana (Boulenger 1920), but later
revised into distinctive genera of Amolops, Nanorana,
and Ombrana (Chen et al. 2005; Dubois 1974; Frost
et al. 2006). The earliest first-hand records related to
morphometrics, life history, and habitat notes of the three
species (Boulenger 1882; Giinther 1860; Jerdon 1870)
are not readily accessible at the present time. While the
recent publication of Schleich and Kastle (2002) is rather
comprehensive, it is still unavailable to many readers due
to the high price of the book (Zug 2004). Shah and Tiwari
(2004) provided little information on the associated
habitats of these sympatric amphibians, like surrounding
vegetation and environmental parameters, but their report
lacks data on egg deposition and tadpole stages. The
IUCN Red List Assessment 2004 has further emphasized
the need for research on the taxonomy, population size,
distribution, trends, ecology, and life history of these
frogs to prioritize conservation actions (Bordoloi et al.
2004; Liang et al. 2004). Therefore, any readily-available
publication on the natural history of these frogs is of great
importance to the scientific community, conservationists,
natural resource managers, and decision makers.
Stream-dwelling frogs serve as good indicators of
the stream ecosystem health, since they are philopatric
Correspondence. * thepristinewoods@gmail.com, biraj@savethefrogs.com; 7 tamumin23@gmail.com
Pp Ss Y S S
Amphib. Reptile Conserv.
November 2019 | Volume 13 | Number 2 | e198
Shrestha and Gurung
Location Map of Manaslu Conservation Area
28°30'0"N 28°40'0"N 28°50'0"N
28°20'0"N
4:1,500,000. ~
84°30'0"E
y 2 > ¥ - ‘ & = =
1:580,000 - pt, a
Coordinate System: GCS WGS 1984 . ;
Datum: WGS 1984 ‘
Units: Degree
as ee
34°40°0"E 84°50'0"E 85°10°0"E
Legend = Village Boundary ---- Road Network z= Manaslu Conservation Area Boundary
Fig. 1. Study sites in Manaslu Conservation Area, Nepal, with villages indicated in blue text.
in nature and found in steady populations (Welsh and
Ollivier 1998). Studying such stream frogs with respect
to morphology, life history, and habitat conditions will
help to further understanding of their ecological niches
(Ningombam 2009). This knowledge is vital for devising
efficient conservation strategies when one-third of the
total amphibian species of the world are being threatened
with extinction (Baillie et al. 2004). This study presents
the natural history notes of these three sympatric frogs.
This information will help to aid in further research and
monitoring, while providing background support for
good decision making regarding their conservation in the
future.
Materials and Methods
Surveys. Manaslu Conservation Area is one of the
protected areas in Nepal, located at the upper north
area of Gorkha district, province number 4 (Gandaki
Pradesh). Surveys were conducted in five major villages
of the Manaslu Conservation Area, namely Sirdibas,
Bihi, Chumchet, Prok, and Samagaun, excluding Lho
and Chhekampar (Fig. 1). The entire survey spanned 49
days during the day-time in April-May 2016 and March
2017.
A distance of 279 km was covered on foot throughout
the survey and a transect of 200 m was walked in each
site of the 14 streams (Table 1). Time-constrained
searches were conducted for 2 h with two people at
a time, for a total of four person-h per search. Live
specimens of Amolops formosus, Nanorana liebigii, and
Ombrana sikimensis were collected for morphological
Amphib. Reptile Conserv.
examination. They were released in-situ after recording
observational notes and taking photographs with a Canon
EOS 700D (18-135 mm) kit lens DSLR camera (Fig. 2).
Egg clutches and tadpoles of different sizes were found
in a few streams, and they were closely observed while
causing minimal disturbance. The distribution of these
sympatric frogs in Manaslu is restricted to Sirdibas, Bihi,
and Chumchet (Fig. 3).
Measurements. The snout-vent length (SVL), head
length (HL), head width (HW), femur length (FL), and
tibia length (TL) were the morphological parameters
measured following Fei et al. (2009) for the adult frogs.
The morphometric keys for tadpoles were total length
(TL), body length (BL), body width (BW), and tail muscle
width (TMW), and followed Mitchell et al. (2012). All
the measurements were taken using a Mitutoyo digital
Vernier caliper to the nearest 0.1 mm.
Air and water temperature measurements were taken
using a digital thermometer. The humidity was measured
using a Hygrometer and the pH of the water was
recorded with a digital pH meter. Geographic coordinates
and altitude were recorded with a Garmin eTrex 10
GPS. Species identification and additional information
followed Boulenger (1882, 1920), Chen et al. (2005),
Frost et al. (2006), Gunther (1860), Ningombam (2009),
Schleich and Kastle (2002), and Shah and Tiwari (2004).
Results and Discussion
Morphometrics. The morphological notes of the
three sympatric frogs correspond well with the earlier
November 2019 | Volume 13 | Number 2 | e198
Three sympatric frogs in Manaslu Conservation Area, Nepal
Table 1. Sampling locations and observations of frogs (adults, egg clutches, and tadpoles) in the survey.
Sampling Site
1
ies)
on nN N
14
Village
Sirdibas
Sirdibas
Sirdibas
Chumchet
Chumchet
Chumchet
Chumchet
Chumchet
Chumchet
Chumchet
Samagaun
Prok
Bihi
Bihi
Location
Yuwang Khola*
Ghatte Khola
Myarchwang
Khola
Gyanak Khola
Sipchet Ripchet
Chumling
Gumlung Khola
Sardi Khola
Lokpa
Phujung Khola
Birendra Tal
Namrung Khola
Bihi Khola
Dyang Khola
Altitude (m asl) Survey Time
1,622
2,425
1,629
2,294
2,473
2,485
2,482
1,938
1,887
1,931
3,700
2,462
2,189
1,838
*K hola refers to stream
descriptions provided by Giinther (1860, 1875) and
Jerdon (1870) quoted in Schleich and Ka4stle (2002).
Nanorana liebigii has the largest mean body size and body
weight followed by Ombrana sikimensis and Amolops
formosus. The body weight measurements of these
frogs found in Nepal did not set new records. In Bhutan,
Wangchuk (2017) documented the average weight of
Nanorana liebigii as exceptionally higher (males 500—
750 g and females 350-500 g) than the present findings
for Nepal. The head lengths (HL) of Amolops formosus
and Nanorana liebigii were smaller than the head widths
(HW), however, Ombrana_ sikimensis was different,
with HL greater than HW (Table 2). On the contrary,
Boulenger (1920) has described broader HW than HL in
Ombrana sikimensis.
Frogs in general tend to exhibit sexual dimorphism,
with females mostly being larger in body size than males
(Monnet and Cherry 2002). The results here agree for
Amolops formosus, where females were larger in size
than males; however, the males of Nanorana liebigii were
Observations
Day Amolops formosus (2 2, 1 4); Nanorana
liebigii (5 tadpoles, egg clutch)
Day None
Day Nanorana liebigii (1 4); Ombrana
sikimensis (7 individuals, unidentified
sex)
Dawn Amolops formosus (3 9); Nanorana
liebigii (1 3)
Day Nanorana liebigii (1 3)
Dawn Nanorana liebigii (1 )
Day None
Dawn Nanorana liebigii (tadpole with
metamorphosed legs)
Day Nanorana liebigii (egg clutch)
Day Nanorana liebigii (1 3)
Day None
Day None
Day Amolops formosus (1 9°); Nanorana
liebigii (1 3)
Night Amolops formosus (1 9)
larger in size than their female counterparts. The adult
males of Amolops formosus had a nuptial pad on the 1*
finger of the forelimb and also partly turquoise-colored
hind limbs on the ventral side (Fig. 4A), as documented
by Schleich and Kastle (2002). Likewise, males of the
Nanorana liebigii had strongly hypertrophied forelimbs
with a nuptial pad on the 1* finger. Further, numerous
black horny spines were present on the 1°, 2" and 3”
fingers on both the arms and extending along the pectoral
region (Fig. 4C). It was difficult to identify the sexes of
Ombrana sikimensis based only on SVL measurements,
since nuptial spines are not present in Ombrana sikimensis
(Boulenger 1920).
Egg deposition and larval stages. Spring (March—
May) is the season of breeding for Nanorana liebigii
as egg clutches were found in slowly drifting Yuwang
Khola in Sirdibas village to fast flowing streams in
Lokpa, Chumchet village. The eggs were attached to the
undersides of stones, totally submerged, and white in
Table 2. Morphological parameters (SVL, HL, HW, FL, and TL) of the three species of adult sympatric frogs (mm) and BW (g). Min
= Minimum value, Max = Maximum value, M = Average value (Mean), SD = Standard Deviation, and n = number of individuals.
Amolops formosus
Morphometric keys (n= 8)
Min M+SD Max Min
Snout-vent length(SVL) 67.3 74.14+3.8 81.5 78.8
Head length (HL) 230. “2a hr 26-1 25.8
Head width (HW) 246 258410 27.9 274
Femur length (FL) 399 429419 461 43.2
Tibia length (TL) 452 475412 49.1 47.6
Body weight (BW) 35 46.9+6.2 55 60
Amphib. Reptile Conserv. 154
Nanorana liebigii Ombrana sikimensis
(n= 6) (n=7)
M+SD Max Min M+SD Max
87.74£7.6 99.6 67.1 81.24 11.6 92.1
27. 9+.2:0 31.5 21.6 24.6°£:2:3 27.1
29.1+1.8 32.4 20.5 233-4592 25.8
50.6 + 3.7 53.1 39.3 44.0+3.9 47.9
54-7439 58.7 42.3 46.44 3.4 50.2
82.84 148 100 50 70.1 + 14.6 85
November 2019 | Volume 13 | Number 2 | e198
Shrestha and Gurung
ite? "ee Ae
be
¥
Fig. 2. Dorsal view of live adults: (A) Ombrana sikimensis, (B) Amolops formosus, and (C) Nanorana liebigii. (D) Dorso-lateral
view of Nanorana liebigii. Photos: Biraj Shrestha and Min Bahadur Gurung.
color inside the gelatinous ball that had a honeycomb-
like appearance (Fig. 5A—B). The clutch size consisted
of about 80-140 eggs although no adults were seen
nearby, which is noteworthy since males of Nanorana
liebigii are reported to guard the eggs as a form of
parental care (Rai 2003). Some gradually developing
egg clutches were observed that had embryos with eyes
and were surrounded by jelly of a “liver-like” color
(Fig. 5C).
Five tadpoles of Nanorana liebigii were observed at
the Yuwang Khola and one metamorphosed tadpole with
hind limbs was evident in the shallow pools of a rapidly
flowing stream in Sardi Khola. The metamorphosed
tadpole had a well-developed oral disc (Fig. 5D), with the
structure of the upper and lower lips forming an atrium
feature (Kastle et al. 2013). The tails of the tadpoles were
nearly twice the length of the body (Schleich and Kastle
2002), while the body lengths were significantly greater
than widths (Table 3).
Tadpoles of Nanorana liebigii were found sympatric
with the tadpoles of Duttaphrynus himlayanus. However,
no egg clutches of Amolops formosus were observed
during the study. Published information on egg deposition
by Amolops formosus is limited, though Nidup et al.
(2016) reported an egg clutch of Amolops himalayanus
attached underneath of rocks and clear white, from a
gentle flowing stream in Bhutan.
Habitat notes. The general habitat ofall the three sympatric
frogs studied here is mountain streams above 1,100 m asl
Amphib. Reptile Conserv.
elevation and of varied intensity. In addition, Nanorana
liebigii was also found to inhabit other water bodies, such
as the puddles in a bamboo forest and irrigation ditches
near the cropland where Karu (a type of naked barley)
was grown (Fig. 6). Amolops formosus preferred fast
flowing streams, typically cascades, attaching themselves
to the steep slopes of rocks and resting on fissures, partly
covered in moss and ferns, while Ombrana_ sikimensis
were typically hiding in clusters underneath rocks in
shallow streams (Fig. 6C). The nearby riparian vegetation
included Nepalese Alder (Alnus nepalensis), Broom
Grass (Thysanolaena maxima), Himalayan Blue Bamboo
(Himalayacalamus hookerianus), Himalayan Silver
Birch (Betula utilis), Tree Rhododendron (Rhododendron
arboreum), Chir Pine (Pinus roxburghii), Walnut (Juglans
Table 3. Morphological parameters (TL, BL, BW, and TMW)
of the tadpoles of Nanorana liebigii (mm). Min = Minimum
value, Max = Maximum value, M = Average value (Mean), SD
= Standard Deviation, and n = number of individuals.
Nanorana liebigii
Morphometric keys Tadpole (n = 6)
Min M+SD Max
Tail length (TL) 414 491+6.7 577
Body length (BL) 13.3 193445 245
Body width (BW) So. GMEG 5 14.7
Tail muscle width (TMW) one Fpeie asl) 1g bs;
November 2019 | Volume 13 | Number 2 | e198
Three sympatric frogs in Manaslu Conservation Area, Nepal
Amphibian Occurrence and Distribution in Manaslu Conservation Area, Gorkha District, Nepal
Samagaun | a
Tee t _
Clq SSere-k Sam
28°39'0"N
28°32'0"N
pani Peak (Lidanai Pefk)
Luksui
E
1:300,000
Apu aQhung ae
aye ree
f aoe pBaibhuk
( Cy Asyarangee”enakhar,
Chumchet \
Seyjae ee aes ¢ (
car i
a Pied ( \ f
Rs ‘
~ gs ae Y Pp x
a
Chhilungkholagaun
28°25'0"N
Ghyachok
® Amolops formosus @ Nanoranaliebigii @
Legend % Duttaphrynus himalayanus
84°30'°0"E
28°18'0"N
_Sirdibas.,.
ae e aatuaees S
84°50°0"E
Ores .)
Masing Now
eWlenore’f
Nagjet 2
sa, Siribas’ my
Local Village Point 4 Metamorphosed Tadpole
Transect
85°10°0"E
Fig. 3. Frog observation sites and distances travelled throughout the survey.
regia), and others.
Amphibians are often mentioned as the bio-indicators
of water quality because of their permeable skin.
Their eggs and larval stages are generally much more
vulnerable to any type of pollution in the water bodies due
to their lack of protective covering, and direct connection
with the water for survival and growth. The optimal
environmental conditions of their habitat are crucial to
allow for metamorphosis and for habitat management
strategies. Cold water is favorable for the growth of
different life stages with neutral to slightly alkaline water
pH. This range is desirable for much of the aquatic fauna,
including stream dwelling frogs, as lower acidic pH
conditions can impede amphibian growth and inhibit the
development of eggs and embryos (Ningombam 2009).
Conservation status. All the three species of frogs are
listed in the Least Concern (LC) category in the IUCN
Red List Assessment from 2004 (15 years prior to this
writing) based upon the presumption of their large
populations, wider distributions, and with no prospects
of immediate decline. However, a reassessment 1s
desperately needed, as the current population trends for
all three species are going down due to declining stream
habitats from various causes, such as water diversion
and dams to deforestation and pollution (Bordoloi et
al. 2004; Liang et al. 2004). In India, all three of these
species are protected under the national legislation, while
no similar effort by the Nepalese government has been
undertaken to provide any legal measures for amphibian
conservation. This remains the case today (in 2019),
despite the recommendation by the Biodiversity Profiles
Amphib. Reptile Conserv.
Project (BPP, 1995) for nine species of endemic Nepalese
amphibians to be included in the Schedule I of National
Parks and Wildlife Conservation (NPWC) Act 1973.
Anurans of genera Amolops, Nanorana, and Ombrana
are called ‘Paha’ frogs in Nepal and have ethnozoological
relationships with the communities living mostly in hills
and mountains (Shah and Tiwari 2004; Shrestha 2018).
People often harvest paha frogs as a delicacy and for
their apparent therapeutic benefits. Every indigenous
community in the mountains of Nepal either has
experience in paha hunting or at least knows about its
use. As a result, paha hunting is popular in villages from
the east to western part, all across the nation. The hunting
usually takes place at night during pre- and post-monsoon
seasons, when the water flow is minimum. There is
no limit for harvested quantities from the streams, and
people usually collect as many as they can find during
their searches. In Manaslu, Gurung communities in
Sirdibas village typically collect 51-100 individuals on
Table 4. Physico-chemical characteristics of water quality in
the survey sites and altitudinal range of the detected frogs. Min
= Minimum value, Max = Maximum value, M = Average value
(Mean), and SD = Standard Deviation.
Abiotic factors Min M+ SD Max
Air Temperature (°C) 8 20.0 + 6.5 26.5
Water Temperature (°C) 4 132-22. 8 16.3
Relative Humidity (%) 25 ASS e117 55
pH cs 8.0+0.3 8.6
Altitude (m asl) 1,591 1,880.5+439.4 2,480
November 2019 | Volume 13 | Number 2 | e198
Shrestha and Gurung
and (D) female of Nanorana liebigii. Photos: Biraj Shrestha.
average in one season and they trade locally in the price
range of USD 0.45—2.26 (Shrestha and Gurung 2019).
Nanorana liebigii is the most popular paha frog across
the country, followed by Ombrana sikimensis which
is highly sought after as its meat serves as a delicacy
and nutritional purposes (Shah and Tiwari 2004). In
addition, the meats of Nanorana liebigii and Amolops
formosus are traditionally assumed to have medicinal
properties that cure fever, cough, cold, dysentery, and
stomach ache; while their skin secretions have antiseptic
properties (Shrestha and Gurung 2019). In recent years,
paha hunting 1s largely practiced to enjoy its meat and for
recreational purposes in the villages, since the nutritional
requirements are often met by poultry and livestock, and
medical supplies are readily available thanks to improved
road access for most villages these days. However, the
continued paha hunting practice has depleted its numbers
as reported by the local communities across the country,
including Manaslu, and has led to the recommendation
for some form of legal conservation protection.
The diminishing populations of Amolops formosus,
Nanorana liebigii, and Ombrana_ sikimensis can be
averted by developing species specific conservation
priority plans. Habitat conservation planning, population
study and monitoring, hunting regulation policies, and
effective outreach programs are some of the key action
steps. The brief natural history notes presented here on
morphometrics, sexual dimorphism, egg deposition,
larval stages, and habitat conditions will be helpful in
this regard. But since the identification of congeneric
amphibians can be tricky, the use of molecular phylogeny
Amphib. Reptile Conserv.
and call identification coupled with morphometrics is
strongly recommended for accurate species identification.
Acknowledgements.—We are thankful to the Rufford
Foundation, UK for funding this research in the first
place. Then, we acknowledge the following institutions
and individuals; SAVE THE FROGS!, Friends of
Nature (FON) Nepal, Department of National Parks and
Wildlife Conservation (DNPWC), National Trust for
Nature Conservation (NTNC) Manaslu Conservation
Area Project (MCAP) Office, Gorkha and Philim, The
Pollination Project (TPP) USA for their technical input
and facilitating this study, approval of the research
permits and support through additional funding. We also
thank Saney Pd Suwal and Mano) Konga who assisted
with the field works, local community of Manaslu for
embracing our mission to protect the paha frogs, Bishnu
Maharjan for producing the GIS maps and Kiran Lohani
for the media exposure. Finally, we value the feedback
received from all the anonymous reviewers and the
journal editorial team (ARC).
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of Threatened Species. A Global Species Assessment.
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Switzerland and Cambridge, United Kingdom. 191 p.
Bordoloi S, Ohler A, Shrestha TK. 2004. Ombrana
sikimensis. The IUCN Red List of Threatened Species
2004: e.T58246A 11757068.
November 2019 | Volume 13 | Number 2 | e198
Three sympatric frogs in Manaslu Conservation Area, Nepal
<
Fig. 5. Life sta es of Nanorana liebigii: (A) eggs deposition underneath a stone, (B) eg: clutch, (C) embryo development, and (D)
Fig. 6. Habitat varieties of the three sympatric frogs: (A) rapidly flowing stream, (B) series of waterfalls inhabited by Amolops
formosus, (C) slow flowing shallow stream, and (D) irrigation ditch. Photos: Biraj Shrestha.
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Bordoloi S, Ohler A, Shrestha TK, Ahmed MF. 2004.
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au Nepal. Bulletin du Museum National d Histoire
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Haddad CFB, de Sa RO, Channing A, Wilkinson M,
Donnellan SC, et al. 2006. The amphibian tree of life.
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Gunther ACLG. 1860. Contribution to the knowledge of
the reptiles of the Himalaya Mountains. Proceedings
of the Zoological Society of London 1860: 148-175.
Jerdon TC. 1870. Notes on Indian herpetology.
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66-85.
Kastle W, Rai K, Schleich H. 2013. Field Guide to
Amphibians and Reptiles of Nepal. ARCO-Nepal,
Munich, Germany. 609 p.
Liang F, Lau MWN, Dutta S, Shrestha TK, Borah MM.
2004. Nanorana liebigii. The IUCN Red List of
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Mitchell T, Alton LA, White CR, Franklin CE. 2012.
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first record of Amolops himalayanus (Anura: Ranidae)
from Bhutan. The Herpetological Bulletin 136: 13-18.
Ningombam B. 2009. Amphibian fauna in and around
Loktak Lake, Manipur, India with reference to the
genus Amolops Gunther. Ph.D. Dissertation, Gauhati
University, Jalukbari, Guwahati, Assam, India.
Rai KR. 2003. Environmental impacts, systematics,
and distribution of herpetofauna from east Nepal.
Ph.D. Dissertation, Tribhuvan University, Kirtipur,
Kathmandu, Nepal.
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of Nepal: Biology, Systematics, Field Guide. First
Edition. A.R.G. Ganter Verlag, Ruggell, (Liechtenstein.
k201ep.
Shah KB, Tiwari S. 2004. Herpetofauna of Nepal: A
Conservation Companion. IUCN Nepal, Kathmandu,
Nepal. 237 p.
Shrestha B. 2018. Amphibian Conservation: Brief
Introduction in the Context of Nepal. The Rufford
Foundation, London, United Kingdom; SAVE THE
FROGS!, Laguna Beach, California, USA; and
Resources Himalaya Foundation, Kathmandu, Nepal.
20 p.
Shrestha B, Gurung MB. 2019. Ethnoherpetological
notes regarding the Paha Frogs and conservation
implications in Manaslu Conservation Area, Gorkha
District, Nepal. Journal of Ethnobiology and
Ethnomedicine 15(1): 23.
Wangchuk S. 2017. Morphometric Study of Mon-Paa
Frog: A Case Study of Dopuchen, Dumtoe and Tendruk
Gewog under Samtse Dzongkhag. Dzongkhag
Forestry Sector, Samtse Dzongkhag, Bhutan. 24 p.
Welsh HH, Ollivier LM. 1998. Stream amphibians as
indicators of ecosystem stress: A case study from
California’s redwoods. Ecological Applications 8(4):
1,118—1,132.
Zug GR. 2004. Book Review: Amphibians and Reptiles
of Nepal: Biology, Systematics, Field Guide.
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Biraj Shrestha has been affiliated with the California-based amphibian conservation non-profit,
SAVE THE FROGS! since 2013. Biraj obtained a Master’s degree in Environmental Science from
Khwopa College, Tribhuvan University (Kathmandu, Nepal) in 2013. He is deeply interested in
the systematics, evolution, phylogenetics, ecology, ethnobiology, and conservation science of
amphibians. Currently, Biraj is pursuing a Master of Science degree (M.S.) in the Coastal Science
and Policy (CSP) program at the University of California, Santa Cruz, California, USA.
Min Bahadur Gurung is a free-lance researcher and life member of the Small Mammals
Conservation and Research Foundation, Nepal. Min has a Bachelor’s degree from Birendra
Multiple Campus and a Master's degree in Zoology from the Central Department of Zoology,
Tribhuvan University, Kathmandu, Nepal. His research interests include distribution, diversity, and
conservation of amphibians, reptiles, birds, and mammals.
November 2019 | Volume 13 | Number 2 | e198
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 160-171 (e200).
Checklist of the amphibians and reptiles of the
Lely Mountains, eastern Suriname
Rawien Jairam
National Zoological Collection of Suriname, Anton de Kom University, Paramaribo, SURINAME
Abstract.—The Lely Mountains in Suriname have been surveyed only a few times by various herpetologists
since 1973, and most recently in June 2016 by three people during six days. The total number of species
recorded from the Lely Mountains is 102, including 46 species of amphibians and 41 species of reptiles in the
2016 surveys, with 15 additional species from the previous survey. Pluviometric conditions were not favorable
during the survey, so more species of amphibians likely remained undetected. The use of only active searches
probably only allowed detection of a portion of the reptile fauna of the massif. Unfavorable weather and the
relatively small area sampled indicate that the diversity of the herpetofauna of the Lely Mountains is probably
far from being completely documented. The presence of roads established for illegal gold mining and other
human structures, such as a communication tower, have caused significant forest degradation.
Keywords. Anura, conservation, herpetofauna, Lacertilia, laterite landscape, new records, Serpentes, South America,
Testudines
Citation: Jairam R. 2019. Checklist of the amphibians and reptiles of the Lely Mountains, eastern Suriname. Amphibian & Reptile Conservation 13(2)
[General Section]: 160—171 (e200).
Copyright: © 2019 Jairam. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 In-
ternational (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows:
official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 18 October 2018; Accepted: 15 May 2019; Published: 14 November 2019
Introduction
Presently the herpetofauna of Suriname consists of
approximately 303 species (Ouboter 2017). Although
over 90% of Suriname is still covered by natural
vegetation, only a few studies have assessed the
herpetofaunal diversity of Suriname throughout the
entire territory (Hoogmoed 1973; Ouboter and Jairam
2012) leaving many areas still unexplored. Herpetofaunal
surveys in specific areas have been conducted by several
researchers (Ouboter et al. 2007, 2011; Nielsen et al.
2013; Fouquet et al. 2015a,b). New country records are
still being documented, e.g., Amapasaurus tetradactylus
(Jairam and Jairam-Doerga 2015), and range extensions
continue to be reported, e.g., Ptvchoglossus brevifrontalis
(Jairam and Jairam-Doerga 2016).
The Lely Mountains are located in the eastern part
of Suriname (4°25’-4°45°N, 54°39’-54°55’W) and
together with the Brownsberg, Nassau, Winti Wai, Hok-
a-Hin, Stonbroekoe, and Majordam Mountains they
form a system of laterite-bauxite plateaus in northeastern
Suriname. These small plateaus form a unique type of
landscape (H. ter Steege, pers. comm.) with different
vegetation types, including high forest, savannah forest,
and rocky creek beds (Alonso and Mol 2007). The Lely
Correspondence. rawien_2000@yahoo.com
Amphib. Reptile Conserv.
Mountains together with the Brownsberg and the Nassau
Mountains comprise a bauxite concession of the Suriname
Aluminum company (Suralco), which formerly operated
in Suriname (Mol et al. 2007). Although Suralco explored
the Lely Mountains for bauxite deposits, the company
did not proceed with the mining exploitation. The Lely
Mountains consist of several plateaus with a maximum
height of approximately 700 m (Alonso and Mol 2007).
Due to the absence of established roads for cars, the Lely
Mountains are mainly accessible only by air. A trail that
is used by gold miners going up the Lely Mountains by
means of all-terrain vehicles is long and tedious, and
seldom without dangers. These circumstances have
led to relatively few surveys (Hoogmoed 1974, 1975,
unpub.; Watling and Ngadino 2007) at this location when
compared to other nearby bauxite mountains, such as the
Brownsberg Mountain. The remoteness of this location
may also favor the occurrence of microendemics and/or
rare species such those as in Anomaloglossus (Vacher et
al. 2017). However, information about the herpetofauna
of the Lely Mountains 1s still scant. This report documents
new findings from the herpetofauna surveyed in the Lely
Mountains in June 2016, and presents an overview of the
herpetofaunal diversity observed and an updated list for
this location.
November 2019 | Volume 13 | Number 2 | e200
Rawien Jairam
pueINs) YOUdI4
of
Legend
— Large creeks
r Rivers
‘(ig Brokopondo Lake
/ ALTITUDE
| j|0
[| 50
100
250
500
750
1000
Fig. 1. Map of the Lely Mountains plateau showing the area surveyed in the red square. The inset image shows the location of the
Lely Mountains in Suriname, as indicated by the red arrow. In the right upper side of the figure the Nassau Mountains are visible.
Materials and Methods
Habitat description. The vegetation and water
drainages in the Lely Mountains are presently heavily
disturbed locally by illegal small-scale gold miners.
Some of the areas sampled were the airstrip, which was
covered with grass, and small ditches located on one
side for water drainage. The area around the airstrip was
surrounded by patches of pristine forest interspersed
with disturbed forests. The vegetation in the disturbed
areas included mostly trees that were approximately
two m high. The cause of this disturbance could have
been the establishment of the airstrip by Suralco. The
Amphib. Reptile Conserv.
bauxite company also established roads that extend from
the plateau to the northern part of the Lely Mountains.
The aforementioned roads were usually dominated by
large water filled potholes bordered by small shrubs and
bushes. Also sampled was a small creek on the plateau,
which was heavily disturbed by artisanal gold mining.
Survey methods. Three people opportunistically
surveyed the forest of the Lely Mountains using available
roads and trails for six days. Trails and roads were surveyed
radiating in different directions from the airstrip (Fig. 1).
The surveyors also walked through the forest away from
trails to increase the chance of finding amphibians and
November 2019 | Volume 13 | Number 2 | e200
Herpetofauna of the Lely Mountains, Suriname
reptiles. Night surveys started at dusk, at approximately
19.00 h, and usually lasted up until 24.00 h into the night.
Amphibians and reptiles were actively searched for and
were collected by hand when encountered. Call records
were made for calling amphibians using a Marantz
recorder with an external microphone. All recorded
calls were analyzed using the software Audacity (http://
audacityteam.org) and compared against currently known
anuran call databases. Pools on the road and in other
potential locations were checked for tadpoles. Searches
for amphibians and reptiles were conducted during
the day. All collected specimens were photographed,
and afterwards were sedated and sacrificed in the field
using Lidocaine®. Specimens were preserved in 10%
formalin (one part full-strength formaldehyde and nine
parts water) and after a few days they were transferred
to 70% ethanol for storage at the National Zoological
Collection of Suriname (NZCS). The identities of some
of the amphibian specimens collected were verified by
molecular analyses, as indicated in Table 1. Additionally,
some data are provided below on the habitats where the
species were collected, and whether they are documented
here for the first time for the Lely Mountains.
Historical survey data. To complete the present list of
species known from the Lely Mountains searches were
performed in the online databases from Naturalis (http://
bioportal.naturalis.nl) and GBIF (https://www.gbif.org/
species/search) to check for species from this location that
were not formally mentioned in the published literature.
Figure 2 gives an overview of the total number of species
documented in the three herpetological surveys at the Lely
Mountains (Hoogmoed in 1974/5, Watling and Ngadino in
2006, and the fieldwork reported here in 2016).
Results
A total of 28 species of amphibians, representing
seven families, and 18 species of reptiles in 11
families, were collected (Figs. 3-8). All specimens
were unambiguously identified to the species level.
Previously, 19 anuran species were recorded for the
Lely Mountains (Watling and Ngadino 2007). The two
lists combined yield a total of 29 species, eight of which
were never before documented for the Lely Mountains.
For the Lely Mountains, the RAP (Rapid Assessment
Program) reported a total of 18 reptile species (Watling
and Ngadino 2007); the present survey also collected
a total of 18 species, seven of which were new records
for this location. Database searches of Naturalis (http://
bioportal.naturalis.nl) and GBIF (https://www.gbif.org/
species/search) provided a total of 34 anuran species, 17
of which were not documented during either the RAP or
the survey held in June 2016. For reptiles, Naturalis and
GBIF yielded a total of 25 species, 13 of which were not
documented in the surveys. Taking into account all of
the surveys and database reports for the Lely Mountains
yields a total of 46 anurans and 41 reptiles identified to
the species level (Table 1).
Some noteworthy observations were made for some of
the amphibian and reptile species collected in June 2016.
* Anomaloglossus stepheni was collected for the first
time in the Lely Mountains. Specimens were collect-
ed in the leaf litter in a patch of dry pristine forest
approximately one km north of the airstrip.
¢ Boana xerophylla is formally reported for the first time
for the Lely Mountains, and was collected during the
Table 1. Amphibian and reptile species reported for Mount Lely, Suriname. Data are included from three main sources: the Rapid
Assessment Program (“RAP 2007”), the current survey conducted in June 2016 (“Current 2016”), and all others from literature
surveys and online sources (“Other”). The latter include literature references, when available, and asterisks indicate the original
collector(s), when known. For species only reported from one of these three sources, the table cells are color coded (yellow, green,
or blue), which emphasizes the inherently “incomplete” nature of any individual survey. The last column (“Seq”) indicates whether
sequences are available.
Hisar taxa eit Current Original collector/literature
8 P se a sen __
[Amphibiamara
a ae)
[Atomobatdee | Allobaresfemoratis | | x | _X | Woogmosa 7s" | X_
[Atomobatidae | Allobares gram | | x | x | Noonanand Gaucher 2005_[_x_
a
Bufonidae Rhinella margaritifera species
complex
Atelopus hoogmoedi — SF Ouboter and Jairam 2012 =
Amphib. Reptile Conserv. 162 November 2019 | Volume 13 | Number 2 | e200
Rawien Jairam
Table 1 (continued). Amphibian and reptile species reported for Mount Lely, Suriname. Data are included from three main sources:
the Rapid Assessment Program (“RAP 2007”), the current survey conducted in June 2016 (“Current 2016”), and all others from
literature surveys and online sources (“Other”). The latter include literature references, when available, and asterisks indicate the
original collector(s), when known. For species only reported from one of these three sources, the table cells are color coded (yellow,
green, or blue), which emphasizes the inherently “incomplete” nature of any individual survey. The last column (“Seq’’) indicates
whether sequences are available.
a
igher taxa epee 2007 | 2016 citation ad
a —— | (a | Cy Cac)
a a
Caste [Beane serpinla |
isiae | Denton excoptens [|X| | Hoge 175
C ivse | Dendopsops mina [| |x| Hoopmecs 1975"
Hylidae Dendropsophus melanargyreus yi 4 Hoogmoed and Avila Pires [|
1991
tiyiase | Dendropsophas gauchers | | [MN Fougueterai 27 [| _
[ivliae | Oseocephas oophagus | | Ia
Ttivliae | Oseocephatusaurims |X | [| _X | Hoogmoed 75" | _
Tfivlidae | Osteocephats teprewt | | [RIN Oubover and Jairam 2072 |
Ttivlidae | Oseocephats tence | | [RIE oogmoed and Poder 1975" [
[Phyttomedusiae | Puhecopus pochondriats [|X | x | _Myersio7s | _
[Phyltomedusidae | Callnedusatomopnerna | |X | _X | Hoogmoea i975" | __
[Phyltomedusidae | Plyllomedusa bicolor | | | _X_| Hoogmoed 975" | X_
[Phyliomedusidee | Plyliomedisa vain | | [IN Hoogmoca 75" [__
a So =
Trias | Sein protoscidens | | MN Hoogmocao7s® |
Triylidae | Sein boesemari____| | ___[N——_Hoogmoea 975" | __
a — aaa
||
Leptodactylidae Adenomera heyeri —- and es 1957:
SSS et al. 2011
ee
js i a
Tceptodaeylidae [Leprodacpiustongirstis | _x [x | | sd
Tceptodactylidae [ Leprodacyius mstaceus | x [x _| _X | Hoognoed and Poder 1975" [__
Tceptodaetylidae | Leprodacyius pentadacyus | x [x |x | Hoogmoed 1975*_ | __
TKeprodacyldae [Lepradacytus senodema | | JRE Hoozmoed ana Myers 1775" |
Tceprodacylidae [Leprodacytus guianensis | [|X |X | Hoogmoed 975 |X
Tceprodacyldae | Leprodactusrhodomystax | | x | _X_| Mooginoed and Poker 1973" |_x_
TLeprodacylidae [Leprodacytus peers | | REN)—Ouborer and Jaram 2012 |
a TY po
[Strabomantiae [Prsimanis ngunatis |__| [RIN Outer and ara 019 |
TStrabomanidae [Prisimanns marmorans |_| __[J———Myers 1975]
SS
[Swabomantiae [Pristmanissps _|_x [x |] Ss
Amphib. Reptile Conserv. 163 November 2019 | Volume 13 | Number 2 | e200
Herpetofauna of the Lely Mountains, Suriname
Table 1 (continued). Amphibian and reptile species reported for Mount Lely, Suriname. Data are included from three main sources:
the Rapid Assessment Program (“RAP 2007”), the current survey conducted in June 2016 (“Current 2016”), and all others from
literature surveys and online sources (“Other”). The latter include literature references, when available, and asterisks indicate the
original collector(s), when known. For species only reported from one of these three sources, the table cells are color coded (yellow,
green, or blue), which emphasizes the inherently “incomplete” nature of any individual survey. The last column (“Seq”) indicates
whether sequences are available.
Hivher taxa Riteiaa Current Original collector/literature
8 P a a seen __
| Amphibia: Anura | Anura
ee! Gee
TStrbomantidee [Pristimants guturais | | __f]—Outover and Jira 2012 [__
Pe A
Amphibia:
eunnonueng
Microcaecilia grandis | Wilkinson et al. 2009 et al. 2009
Total amphibians 49 species 19 28 33
[ReptarSawria [SC SSE Crd dTTCCSCSdr
[Phyllodciyliae | Thecadachs rapid = a ae
TGekkonidee | Lepiodacttus ngubris | _ I
TGekkonidae | Hemidacyus mabouia [___ a
i
[sphaerodacylidae | Gonatodes hamerais _[_X [x | _X | Hoogmoes 7 [
[Gymnnoptaimidae | Loxopholisganense [x [x | _X | Hoogmoea ior _[
[Gyinoptaimidae | Nenscuras bcurinarus [| x _| _X__| Hoogioed and Polder 1975" | __
[Gymnoptaimidae [.Nensticurasruds | _X [| X | Hoogmoea v7" _[
Gymnopthalmidae Arthrosaura reticulata Hoogmoed and Avila-Pires
1992
Gymnopthalmidae Arthrosaura kocki xX xX Hoogmoed and Avila-Pires
1992
1992
[Daciyloitae | Anotischrwoteps | x | | _x_ | Hoogmoed io75" | _
TDactyloitee | Anotispunctans | | [RI Hoogmoea 975" | _
[Potyehrotae | Pobyohras marmoranns | |
[ Seinciae | Copecglossum nigropuncranm | x |__| X | Hoogmoed 75" | __
[Gyinnophaimidae [iphisactegans |_| [RIN Hoogmoea 975° | __
TGyinnophthamidae | Treoscinensagiis | | [MN —_Hoogmoea 975" | __
TSpacrodaciylidae | Chuogetto amaconicus | | [MN] Hoogmoea 975" [| _
teidee —___[Ameivaamena | x |X | _X_ | Hoogmoea i975" | _
[reine | Papinambisegutsin | x |x [| ———s+ds
[tropiauridae | Plcaplica __—————~it x ‘|| x | GkMesm | _
[tropiduidae [Plea umbra | | | x | Hoogmeedi975* | __
Repti: Crocodyia | Ci CT TT Cd
[Alligatrdse | Paleonuchus rigonans | x |x [| |————s+dts
TAllgatordae [Caiman crocodius | | [NN] —_Hoognoeaionse | __
Repti serpents | PT CSC
[ Leptotyphopidae | Stagonodon capmensts | | [IN Hoognocaio77 | __
[ceptotyphopidae [Apia enetta =i So —
Amphib. Reptile Conserv. 164 November 2019 | Volume 13 | Number 2 | e200
Rawien Jairam
Table 1 (continued). Amphibian and reptile species reported for Mount Lely, Suriname. Data are included from three main sources:
the Rapid Assessment Program (“RAP 2007”), the current survey conducted in June 2016 (“Current 2016”), and all others from
literature surveys and online sources (“Other”). The latter include literature references, when available, and asterisks indicate the
original collector(s), when known. For species only reported from one of these three sources, the table cells are color coded (yellow,
green, or blue), which emphasizes the inherently “incomplete” nature of any individual survey. The last column (“Seq”) indicates
whether sequences are available.
Thieher taxa Sanins Current Original collector/literature
8 P site a Stren _
Repti Semenes
Sa a | a ee
poids | Corals canis | | EN GEMees 97" | __
Tcoutridae | Atractus badius | | [IN Hoogmoca i975" [| __
[Colutridae | Mastigodryas Boddoer | sc
[Cowbridae | Chironus carinaus | a
Tcowbridae | Chironiusfwcs i? | Orv |
eS a a ie
[Vipers __[Bortropsarox +t x ‘|x [| | sSsSsSsSsd—sS
Vipers [Bothrops brass ————~| | i tndeman os" |
—
PReptitiasTetuaines | YC TCS
[ Cheldse | Platenpplaycephala | x | x |X | Woogoeaio7® | _
SR
Total reptiles 42 species
June 2016 survey. All specimens observed were found ground in a habitat of undisturbed forest.
around the houses on water tanks and rain gauges at the
airstrip. Although this species was observed and possi- ¢ Pristimantis sp. 4 is noted for the first time for the
bly collected by the members of the RAP, the specimens Lely Mountains.
were misidentified as an undescribed Pristimantis spe-
cies. For example, a misidentified specimen is depicted
° Thecadactylus rapicauda was found on some of the
on the cover of the RAP report (Alonso and Mol 2007).
buildings at the airstrip, apparently having moved to
these locations from the surrounding forests.
* Osteocephalus oophagus was heard calling while
surveyors were walking at night in a patch of un-
disturbed forest south of the airfield in the Lely
Mountains.
¢ Lepidodactylus lugubris is an introduced SE Asian
gecko (Hoogmoed and Avila-Pires 2015), and was
most probably introduced into the Lely Mountains
by the frequent flights which supply the small-scale
time for the Lely Mountains. Specimens were ob-
served on the large water holding tanks found around
yn ¢ Hemidactylus mabouia represents the first record for
the houses on the airstrip.
yet another introduced species in the Lely Moun-
tains, and was frequently observed on the building
¢ A specimen of Chironius carinatus was collected where the surveyors stayed.
near one of the buildings at the airstrip on the tap of
one of the water tanks. ¢ Polychrus marmoratus was collected for the first
time for this location, near the edge of the airstrip.
*A specimen of Trachycephalus typhonius was col-
lected during a night survey while surveyors were
walking on a Suralco road. The collected individual
was sitting on a leaf approximately 1.5 m above the
¢ Two specimens of Epictia tenella were collected in
the morning around 8 AM, while the surveyors were
walking around the edges of the airstrip. Both speci-
Amphib. Reptile Conserv. 165 November 2019 | Volume 13 | Number 2 | e200
Herpetofauna of the Lely Mountains, Suriname
mens were near the grassy edges of the airstrip and
were active when observed.
° Mastigodryas boddaerti was observed whilst lifting
a corrugated plate left behind in one of the aban-
@ Amphibians
ages doned small-scale miner camps.
*The pristine forests around the airstrip contained
relatively large, water-filled depressions which were
attractive to species such as Chiasmocleis shudika-
i Hes PANEL OUEL LON rensis and Platemys platycephala.
Fig. 2. Total number of species per group collected during
each of the major surveys in the Lely Mountains, Suriname. * Roads on the plateau with large water-filled potholes
“RAP” is the Rapid Assessment Program survey (Alonso and
Mol 2007); “Jun-16” is the current survey; “Other collectors”
includes all other available data.
were an ideal habitat for Phyllomedusa bicolor, Cal-
limedusa tomopterna, Pithecopus hypochondrialis,
and other Hylidae.
aE .< ie
;
Fig. 3. (A) Anomaloglossus stepheni; (B) Allobates femoralis;, (C) Allobates granti; (D) Rhinella martyi;, (E) Boana xerophylla,
and (F) Scinax ruber.
Amphib. Reptile Conserv. 166 November 2019 | Volume 13 | Number 2 | e200
Rawien Jairam
:
ove . : "
Recs; ]
o*
“ :
; “oy ei .
. .
S. 3
*N ~ ec? ‘ }
SS ; ‘, mes - — —-
‘es!
, am °
a wu a
Fig. 4, (A) Trachycephalus typhonius, (B) Leptodactylus knudseni (juv.); (C) Leptodactylus pentadactylus (juv.); (D) Leptodactyl us
mystaceus, (E) Leptodactylus rhodomystax (juv.); and (F) Ameerega trivittata.
Discussion
Some problems were encountered with two of the species
collected during the RAP, namely Anomaloglossus
beebei and Anomaloglossus degranvillei. The authors of
the RAP survey confused A. beebei with Allobates granti,
which occurs in the Lely Mountains whilst the former is
only found at Kaieteur National Park, Guyana (Kok et
al. 2006). The Anomaloglossus degranvillei reportedly
collected during the RAP might have been confused with
A. stepheni or A. surinamensis. A study by Fouquet et
al. (2018) has shown that A. degranvillei is restricted to
a small area in French Guiana and also proved that A.
surinamensis probably occurs in the Lely Mountains.
Specimens of A. stepheni were collected during the 2016
survey. Anomaloglossus surinamensis was first described
Amphib. Reptile Conserv.
by Ouboter and Jairam (2012) who had previously also
identified specimens from the nearby Nassau Mountains
as A. degranvillei (Ouboter et al. 2007).
Some of the Pristimantis species documented during
the RAP still remain to be identified, so chances are that
their eventual identification might change the number
of amphibian species for the Lely Mountains. Since the
2016 survey was held in a period with very little rainfall,
very few frogs were calling. Therefore, we believe that
additional surveys during the rainy season would be
interesting and would definitely increase the number of
known amphibians for this location.
The increasing human presence in the Lely
Mountains might have resulted in an extension of the
distribution ranges for Boana sclerophylla, Scinax ruber,
Trachycephallus typhonius, Lepidodactylus lugubris, and
November 2019 | Volume 13 | Number 2 | e200
Herpetofauna of the Lely Mountains, Suriname
Hemidactylus mabouia; species that were not recorded
during the earlier surveys. Although most of the days
spent on the Lely Mountains were quite dry not many
reptile species were collected. Snakes, for example, were
the least represented group, and just four specimens
belonging to three species were found. Small-scale gold
miners were very active in the Lely Mountains, a factor
which might have contributed to the disturbance in the
forest and the only creek that was found and sampled.
The number of species added to the list published during
the RAP and the prospects for organizing another survey
to this location validate the value of this checklist. We
would strongly recommend that the Lely Mountains
be spared from further destruction by illegal mining
activities, and additional surveys involving other groups
should be conducted to establish a satisfactory list
Amphib. Reptile Conserv.
Fig. 5. (A) Leptodactylus longirostris, (B) Boana boans; (C)
Callimedusa tomopterna, (D) Phyllomedusa bicolor, and (E)
Pithecopus hypochondrialis. Photos by D. Baeta.
of species present and to save this Mountain from the
complete destruction of its habitats.
Conclusions
The compiled results presented herein show that the
amphibian and reptile communities on the Lely Mountains
are much more diverse than previously reported. Though
five separate surveys have been conducted at this locality,
chances are that the known species diversity will continue
to increase as different areas on the plateau are surveyed.
The presence of illegal small-scale gold miners on the
plateau has resulted in the rapid conversion of forested
areas into unsuitable habitats which may translate into a
loss of species diversity.
Acknowledgements.—| would like to thank the Nature
Conservation Department that kindly provided the
permits which allowed the fieldwork in the Lely
Mountains. D. Baéta and T. Gazoni were valuable
companions in the field, and contributed significantly
to the number of species documented during the survey
in June 2016. A first draft of this article was reviewed
by A. Fouquet whose comments greatly improved the
manuscript.
November 2019 | Volume 13 | Number 2 | e200
Rawien Jairam
eet eT dies ata
RS ~ Peay ects, OF RE ee
we >: SS
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Fig. 9. Overview of the airstrip in the Lely Mountains with parts of the forest visible where the June 2016 surveys were conducted.
Photo by T. Gazoni.
Rawien Jairam is an associate researcher working at the National Zoological Collection of
Suriname. Rawien has an M.Sc. in conservation biology and has been interested in the herpetofauna
of Suriname for many years. In addition to herpetology in general, he is specifically interested in
taxonomy, species descriptions, and distribution.
November 2019 | Volume 13 | Number 2 | e200
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 172-173 (e201).
Book Review
Islands and Snakes: Isolation and Adaptive Evolution
Bayard H. Brattstrom
Horned Lizard Ranch, P.O. Box 166, Wikieup, Arizona 85360, USA
Keywords. Behavior, biogeography, ecology, reproduction, reptiles, Serpentes, Squamata
Citation: Brattstrom BH. 2019. Book review—Islands and Snakes: Isolation and Adaptive Evolution. Amphibian & Reptile Conservation 13(2) [General
Section]: 172-173 (e201).
Copyright: © 2019 Brattstrom. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 26 September 2019; Accepted: 26 September 2019; Published: 16 November 2019
Snakes on islands, what could make a herpetologist
happier? Islands and Snakes, edited by Harvey B.
Lillywhite and Marcio Martins, is a fun and important | hh ‘
book, with something new and fascinating in every | NSS ae BB By a, e
chapter: A tropical island with Sea Kraits coming ashore i fa aaa
to drink fresh water and to lay their eggs; a sandy Florida
beach, where at the back-beach vegetation, dozens of
Cottonmouth Moccasins wait for falling baby birds or for
the dropped fish that the parent birds had brought to their
young. That and so much more is here in this exciting
book!
Islands are fascinating, as each has its own ecology.
Isolated and oceanic islands have depauperate faunas
due to distance and dispersal. Continental islands have
fairly normal ecosystems, though some species may be
missing and others becoming dominant. The authors of
the chapters in this book show how interesting snakes on
islands have become.
The introductory chapter by Marcio Martins and
Harvey Lillywhite discusses the geology, geography,
and evolution of islands and their snake fauna, followed
by Harold Heatwole’s chapter on the biogeography of
Sea Kraits, and then the chapter by Xavier Bonnet and
Francois Brischoux on Sea Krait behavior, distribution,
and abundance. Fun facts: Sea Kraits can pick up one-
fifth of their oxygen through their skin, they eat mostly
eels, they must go ashore on islands to lay their eggs, they Edited by
form big mating balls, and many have predatory ticks. Harvey B. Lillywhite
In Chapter 4, by Ming-Chung Tu and Harvey ad Marcio Martins
Lillywhite, we learn more about the diving responses of
Sea Kraits and the fact that after a rain, Kraits can drink
from the tiny layer of freshwater that has fallen on the Title: Islands and Snakes: Isolation and Adaptive Evolution
ocean surface...and you will also learn more about the
mating balls.
In Chapter 5, by Marcio Martins, Ricardo J. Sawaya, - Copyright: 2019
Selma Almeida-Santos, and Otavio A.V. Marqués, we JS BN: 978-0-19-067641-4
learn about the ecology of the Lancehead, Bothrops
Editors: Harvey B. Lillywhite and Marcio Martins
Publisher: Oxford University Press
Correspondence. bayard@hughes.net Pages: xii + 343; Price: USD $120
Amphib. Reptile Conserv. 172 November 2019 | Volume 13 | Number 2 | e201
Brattstrom
insularis, on a Brazilian Island; followed by Chapter 6
by Fabien Aubret on the elapid Tiger Snake, Notechis
scutatus, on one of the islands between Australia and
Tasmania, which is the breeding site of several species
of sea birds. With all this available food (shearwaters,
petrels, gulls, cormorants, skinks, and mice), these
snakes get to be as large as 1.5 m and become a hazard
for the scientists that are studying the birds!
In Chapter 7 by Robert Henderson we learn about the
Tree Boa, Corallus grenadensis, followed in Chapter
8 by a study of the ecology and variation in the Milos
Viper, Macrovipera schwizeri, by Goran Nilson.
Chapter 9, by Harvey Lillywhite and Coleman Sheehy
III, continues the important studies on Cottonmouth
Moccasins, Agkistrodon piscivorus, including their eating
baby birds and dropped fish on an island off the coast of
Florida, USA. Richard B. King and Kristin M. Stanford
bring us up to date in Chapter 11 on the decades-long
studies on Water Snakes, Nerodia sipedon insularum,
their ecology, and evolution on Lake Erie islands between
Amphib. Reptile Conserv.
173
the USA and Canada, showing both positive and negative
human impacts on the snakes.
On Catalina Island in the Gulf of California, there
is a rattlesnake that has no rattle, Crotalus catalinensis,
and Chapter 10 by Gustavo Arnaud and Marcio Martins
covers this snake’s behavior, ecology, and conservation;
and suggests that a native Night Snake, Hypsiglena
catalinae, might be a color mimic of this rattle-less
rattlesnake. Chapter 12, by Akira Mori, H. Ota, and
Koichi Hirate discusses the impact of snakes eating
baby sea turtles that are on their way from the nest to the
sea. Since there are “islands” of habitat (deserts, ponds,
areas between lava flows or between rivers), D. Bruce
Means and César Barrio-Amoroés discuss in Chapter
13 the snakes on the South American Sky Islands—the
Tepuis—with interesting results.
Bottom line: The book 1s well written by all the authors,
the pictures are for the most part quite good, and the
information is fun and exciting. BUY IT!
Bayard H. Brattstrom is Professor of Zoology, Emeritus, California State
University, Fullerton. Bayard is the author of over 300 scientific publications,
600 environmental and consulting reports, and nine books. He has been a Visiting
Professor at several Australian Universities and even studied snakes on Clarion
Island, Islas Revillagigedos, Mexico. Bayard currently lives in a solar-based
straw-bale house on top of a hill, south of Wikieup, Arizona.
November 2019 | Volume 13 | Number 2 | e201
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 174-180 (e202).
Possible hybridization between East Pacific Green
Chelonia mydas and Olive Ridley Lepidochelys olivacea
sea turtles in northwest Mexico
12.*Catherine E. Hart, '2°Cesar P. Ley-Quiionez, ‘F. Alberto Abreu-Grobois, °Luis Javier Plata-Rosas,
$Israel Llamas-Gonzalez, ‘Delia Karen E. Oceguera-Camacho, and '?7Alan A. Zavala-Norzagaray
'Grupo Tortuguero de las Californias A.C., La Paz, Baja California Sur, MEXICO *Investigacion, Capacitacion y Soluciones Ambientales y Sociales
A.C. (ICSAS), Tepic, Nayarit, MEXICO +Instituto Politécnico Nacional, CIIDIR Unidad Sinaloa, Guasave, Sinaloa, MEXICO *Laboratorio de
Genética y Banco de Informacion sobre Tortugas Marinas (BITMAR) Unidad Académica Mazatlan Instituto de Ciencias del Mar y Limnologia
UNAM, Mazatlan, Sinaloa, MEXICO *Centro Universitario de la Costa, Universidad de Guadalajara, Puerto Vallarta, Jalisco, MEXICO °Eco
Mayto A.C. Playa Mayto, Cabo Corrientes, Jalisco, MEXICO
Abstract.—Photographic records of sea turtle neonates and embryos which show characteristics of both East
Pacific Green Sea Turtles (Chelonia mydas) and Olive Ridley Sea Turtles (Lepidochelys olivacea) are presented.
These turtles were produced from nests laid by Olive Ridley females in the states of Nayarit, Jalisco, and Baja
California Sur. Their discovery further suggests the occurrence of hybridization between these two species,
and potential implications for conservation are discussed.
Keywords. Black sea turtle, Gulf of California, morphology, conservation, hybrid, Testudines
Citation: Hart CE, Ley-Qufonez CP, Abreu-Grobois FA, Plata-Rosas LJ, Llamas-Gonzalez |, Oceguera-Camacho DKE, Zavala-Norzagaray AA.
2019. Possible hybridization between East Pacific Green Chelonia mydas and Olive Ridley Lepidochelys olivacea sea turtles in northwest Mexico.
Amphibian & Reptile Conservation 13(2) [General Section]: 174-180 (e202).
Copyright: © 2019 Hart et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0
International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any me-
dium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as
follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 24 April 2017; Accepted: 13 July 2018; Published: 19 November 2019
Introduction
Sea turtles are widely distributed throughout tropical
and subtropical oceans. They nest on sandy beaches
throughout their range, and while different species can
be found sharing habitats worldwide each has adapted to
take advantage of different ecological niches (Tomas et
al. 2001; Ballorain et al. 2010; Jones et al. 2012). Despite
this, where species of the same lineage coincide in time and
space mating and inter-specific hybridization sometimes
occurs naturally, a process which influences 25% of
plant and 10% of animal species (Arnold 1997). When
hybridization involves threatened or endangered species
it is considered to be of conservation concern (Allendorf
et al. 2001), and there is a need to determine whether
these events are a result of anthropogenic factors before
implementing management strategies (Genovart 2009).
Of the seven extant species of sea turtles, hybridization
has been reported between Loggerheads (Caretta caretta)
and Kemp’s (Lepidochelys kempii) [Barber et al. 2003];
Loggerheads and Hawksbills (Eretmochelys imbricata)
[Lara-Ruiz et al. 2006]; Greens (Chelonia mydas) and
Loggerheads (James et al. 2004); Greens and Hawksbills
(Seminoff et al. 2003; Kelez et al. 2016); and Hawksbills
and Olive Ridleys (LZ. olivacea) [Lara-Ruiz et al. 2006].
Thus, the Carettini and Chelonini tribes to which they
belong are thought to be one of the oldest vertebrate
lineages that is known to hybridize in nature (Karl et al.
1995), sharing a common ancestor more than 50 million
yr ago (Bowen et al. 1993; Dutton et al. 1996).
Along the Pacific coast of Mexico, nesting occurs
for four species of sea turtles: Leatherback, Hawksbill,
Green, and Olive Ridley, with the latter being by far the
most abundant. East Pacific Green Turtles are the second
most abundant turtle to nest on Mexico’s Pacific beaches,
and they often nest alongside Olive Ridleys. These two
species have overlapping breeding seasons with Olive
Ridleys nesting from May to December (Garcia et al.
2003) and Greens from September to January (Alvarado-
Diaz et al. 2003). Currently both species exhibit incipient
recovery and nearly year-round nesting as a result of the
population increases following decades of conservation
activities. Extensive hunting and egg collection, which
reached industrial levels in the 1970s and 1980s, led
to drastic population declines (Chassin-Noria et al.
2004; Rodriguez-Zarate et al. 2013). These declines
Correspondence. cehart03@gmail.com (*CEH), cleyg@ipn.mx (CPLQ), alberto.abreu@ola.icmyl.unam.mx (FAAG), ljplata@yahoo.com
(LJPR), israel_llamas@hotmail.com (ILG), karen@grupotortuguero.org (DKEOC), anorzaga@ipn.mx (AAZN)
Amphib. Reptile Conserv.
November 2019 | Volume 13 | Number 2 | e202
Hart et al.
Gulf of
California
20°N
Pacific Ocean
110°W
Sinaloa
MEXICO
Nayarit
Islas
Marias |
R
e Playa Chila
Playa El Naranjo
Playa San Francisco
@ Playa El Salado
Playa Mayto
Playa Careyeros
Jalisco
105°W
Fig. 1. Northwest Mexico. Circles denote nesting beaches where suspected hybrid hatchlings have been observed.
were reversed with a total ban on sea turtle use starting
in 1990 (Marquez et al. 1998) and the proliferation of
conservation programs. Improvements in the conditions
of these species have resulted in both being moved from
the Endangered to Vulnerable classifications on the
IUCN Red List, although both species remain listed in
Appendix I of CITES (2007).
Here, the possible hybridization of East Pacific Green
Sea Turtles and Olive Ridley Turtles is reported in
northwest Mexico based on hatchling characteristics.
Materials and Methods
During 2010-2012, hatchlings and embryos from
12 nests laid by different Olive Ridley females were
observed with characteristics (see Table 1) typically
associated with East Pacific Green Turtles. Conservation
biologists collaborating with two NGOs in north-west
Mexico, Red Tortuguera A.C. and Grupo Tortuguero de
las Californias A.C., were requested to report embryos
and neonates that were atypically pigmented, or those
that presented scute or morphological patterns associated
Amphib. Reptile Conserv.
with a species different than that of the female which had
nested. Following the subsequent reports, photographic
records of the neonates were made prior to their release.
Results
All of the hatchling sea turtles that presented atypical
characteristics hatched from nests verified to be laid
by Olive Ridley females. Figures 2A and 2B show the
contrasting morphology and coloration of the carapace
and plastron for Olive Ridley and East Pacific Green
Turtle hatchlings, respectively. Embryos (Fig. 3)
and hatchlings (Figs. 4-5) were occasionally found
presenting coloration typical of East Pacific green turtle
hatchlings. Interestingly these hatchlings were often
the only abnormal hatchlings from an otherwise typical
Olive Ridley clutch, with their siblings presenting typical
Olive Ridley coloration.
Olive Ridley hatchlings presenting a white border to
the marginal scutes and white edges to the flippers were
frequently reported (Fig. 6). We consider this to be a
normal characteristic, and not a sign of hybridization, that
November 2019 | Volume 13 | Number 2 | e202
Possible hybridization of Chelonia mydas and Lepidochelys olivacea
1 =
=
FS a Se Pes ee 3:
~ Ps)
Fig. 2. Carapace (A) and plastron (B) of
A
White
plastron Black
carapace
Fig. 3. Embryo from an Olive Ridley nest, clearly displaying East Pacific Green Turtle coloration on both (A) plastron and flippers,
and (B) carapace. Photos by C.E. Hart.
Table 1. Morphological features of putative hybrid neonate turtles compared to those usually reported for Lepidochelys olivacea
and Chelonia mydas.
Morphological feature L. olivacea C. mydas Putative hybrids
Prefrontal scales 4 2 2 or 4
Post orbital scales 3 =, 3
Marginal scutes 12 11 11-12
Supracaudal scutes 2 2 2
Intergular scute Yes
Postanal scute No
Nuchal scute Yes Yes NES
Lateral scutes 6-9* 4 4-8
Vertebral scutes 6-9 5 6-7
Inframarginal scutes
Keels Yes No Yes
Beak Triangular Rounded, large Triangular or rounded
Anterior claws 2 1 1-2
Carapace color Gray Black Dark gray or black
Plastron color Gray White White
*occasionally five
Amphib. Reptile Conserv. 176 November 2019 | Volume 13 | Number 2 | e202
Hart et al.
Keels on carapace
White border to
marginals and flippers
C
Fig. 4. Deceased hatchling presenting (A) white coloration to the carapace and flipper border, and (B) the white plastron characteristic
of East Pacific Green Turtles, while presenting (C) a typical Olive Ridley carapace and head. Photos by C.E. Hart.
| eC
¥ LA
‘
oe
a
a
P aot -
Fig. 5. Healthy neonate turtles presenting characteristics of both East Pacific Green and Olive Ridley Turtles photographed before
release. Photos by C.E. Hart (A) and F- Sanchez (B).
is present in some but not all Olive Ridley neonates and Turtle neonates, and they have not been described as
is found within all participating hatcheries in southern —_ pigmentation for Olive Ridley neonates. Genetic studies
Nayarit and north Jalisco. However, a white border are needed to clarify whether these neonates are pure
on the marginal scutes and white edges to the flippers | Olive Ridleys or the result of hybridization.
are characteristics associated with East Pacific Green
Amphib. Reptile Conserv. 177 November 2019 | Volume 13 | Number 2 | e202
Possible hybridization of Chelonia mydas and Lepidochelys olivacea
Discussion
Olive Ridley turtles are the most abundant of all sea
turtle species, and this is particularly evident in the East
Pacific, with an estimated 1.39 million large juvenile and
adult Olive Ridley turtles in the Tropical East Pacific
(Eguchi et al. 2007). Because the vast differences in
abundance would greatly increase the opportunities for
hybridization of Olive Ridleys with East Pacific Green
Turtles, there is concern that if these become widespread
they could jeopardize the recovery of the much smaller
East Pacific Green Turtle population. For example,
hybrids could be sterile and so reduce overall fertility.
Hawksbill-Loggerhead hybrids have been found to be
fertile in Brazil where introgression (breeding of hybrids
with one or both parental taxa) has become significant
(Lara-Ruiz et al. 2006). Furthermore, Soares et al. (2017)
found that Loggerhead-Hawksbill hybrids were at no
reproductive disadvantage relative to the pure Hawksbills
among which they nested, suggesting that these hybrids
are likely to persist there.
Many studies report either sterility or low fitness in
hybrids (Allendorf et al. 2001). However, reports from
conservation projects in northwest Mexico suggest that
putative Olive Ridley-Green Turtle hybrid hatchlings are
Amphib. Reptile Conserv.
Fig. 6. Olive Ridley neonate from
Nayarit with the commonly found
coloration of fine white border to
carapace and fore flippers. This
coloration is not reported in the
literature for this species. Photos by
C.E. Hart.
more fit (being first to the water on release) than the Olive
Ridley turtles that hatch from the same and/or different
nests. However, the report of a more aggressive behavior
by some of these hybrid hatchlings is also worrying.
We recommend using these illustrations to aid a
national program aimed at compiling information on
the frequency and locations of occurrence of atypical
hatchlings within conservation projects, in order to
gauge the importance of this phenomenon, coupled with
genetic analyses to definitively confirm hybridization.
If confirmed hybridization is found to be abundant,
possible impacts on the regional populations are a
cause for concern. We hope this information will open
the conversation on the issue of hybridization between
sea turtle species in Mexico and highlight the need
for appropriate management guidelines to advise
conservation projects on the action to take (if any) when
these neonates occur.
Acknowledgments —CEH would like to thank the
Consejo Nacional de Ciencia y Tecnologia (CONACYT)
Mexico for support through a Ph.D. Scholarship
(number 310163). We would also like to thank the many
Tortugueros who have been keeping an eye out for
“strange hatchlings.”
November 2019 | Volume 13 | Number 2 | e202
Hart et al.
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Allendorf FW, Leary RF, Spruell P, Wenburg JK. 2001.
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2003. Clutch frequency of the Michoacan Green Sea
Turtle. Journal of Herpetology 37. 183-185.
Arnold ML. 1997. Natural Hybridization and Evolution.
Oxford University Press, Oxford, United Kindgom. 215 p.
Ballorain K, Ciccione S, Bourjea J, Grizel H, Enstipp
M, Georges JY. 2010. Habitat use of a multispecific
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Chassin-Noria O, Abreu-Grobois A, Dutton PH, Oyama
K. 2004. Conservation genetics of the East Pacific
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Mexico. Genetica 121: 195-206.
Dutton PH, Davis SK, Guerra T, Owens D. 1996.
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on sequences of the ND4-leucine tRNA and
control regions of mitochondrial DNA. Molecular
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Eguchi T, Gerrodette T, Pitman RL, Seminoff JA, Dutton
PH. 2007. At-sea density and abundance estimates of
the Olive Ridley Turtle Lepidochelys olivacea in the
eastern tropical Pacific. Endangered Species Research
3: 191-203.
Espinosa-Carreon TL, Valez-Holguin JE. 2007. Gulf
of California interannual chlorophyll variability.
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Garcia A, Ceballos G, Adaya R. 2003. Intensive beach
management as an improved sea turtle conservation
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Genovart M. 2009. Natural hybridization and
conservation. Biodiversity Conservation 18: 1,435—
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between a Green Turtle, Chelonia mydas, and
Loggerhead Turtle, Caretta caretta, and the first
record of a Green Turtle in Atlantic Canada. The
Canadian Field-Naturalist 118: 579-582.
Jones MEH, Werneburg I, Curtis N, Penrose R, O’ Higgins
P, Fagan MJ, Evans SE. 2012. The head and neck
anatomy of sea turtles (Cryptodira: Chelonioidea) and
skull shape in Testudines. PLoS One 7: e47852.
Karl SA, Bowen BW, Avise JC. 1995. Hybridization
among the ancient mariners: characterization of
marine turtle hybrids with molecular genetic assays.
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Kelez, S, Velez-Zuazo X, Pacheco AS. 2016. First record
of hybridization between Green Chelonia mydas and
Hawksbill Eretmochelys imbricata sea turtles in the
Southeast Pacific. PeerJ 4: e1712.
Lara-Ruiz P, Lopez GG, Santos FR, Soares LS. 2006.
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(Eretmochelys imbricata) nesting in Brazil revealed
by mtDNA analyses. Conservation Genetics 7(5):
773-781.
Marquez R, Jiménez MC, Carrasco MA, Villanueva
NA. 1998. Comentarios acerca de las tendencias
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Seminoff JA, Karl SA, Schwartz T, Resendiz A. 2003.
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and Hawksbill Turtle (Eretmochelys imbricata) in the
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in the directionality of crosses. Bulletin of Marine
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Santos FR, dei Marcovaldi MAG, Byjorndal KA.
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November 2019 | Volume 13 | Number 2 | e202
Possible hybridization of Chelonia mydas and Lepidochelys olivacea
Amphib. Reptile Conserv.
Catherine E. Hart is a marine biologist currently completing her Ph.D. at the Centro Universitario de
la Costa, Universidad de Guadalajara, Mexico. Catherine received her B.S. from Instituto Tecnoloégico
de Bahia de Banderas, and her M.Sc. in Conservation and Biodiversity from the University of Exeter
(United Kingdom). She currently coordinates the Red Tortuguera A.C. and is an adviser on sea turtle
nesting for Grupo Tortuguero de las Californias A.C. Catherine’s current interests include the effects of
temperature and incubation techniques on sea turtle embryos and neonates, and the role that community
groups play in the conservation of sea turtles in northwest Mexico. Photo by C.P. Ley-Quifionez.
César P. Ley-Quifiénez is a Research Scientist and Technician at the National Polytechnic Institute
CIIDIR-Sinaloa, Mexico. César’s research focuses on ecotoxicology and wildlife conservation. He
holds a Ph.D. degree from Universidad Autonoma de Sinaloa, Mexico. Photo by C.P. Ley-Quifionez.
Alberto Abreu-Grobois is a Research Scientist at the Instituto de Ciencias del Mar y Limnologia
(ICML), Universidad Nacional Autonoma de México. Alberto received his Ph.D. in Population
Genetics from University College Swansea, Wales, United Kingdom, in 1983. Since then he has worked
at the Mazatlan Research Station of the ICML where he heads the Genetics Laboratory. Alberto’s
research focuses on the conservation genetics of sea turtle populations and on the temperature effects on
morphometrics and fitness of sea turtle hatchlings. Photo by Raquel Brisefio.
Luis Javier Plata-Rosas has a Ph.D. in Coastal Oceanography and is a lecturer at the University of
Guadalajara, Mexico. Luis has authored more than 600 popular science articles and several books,
including: The Physics of the Coyote and the Road Runner (2016), Myths of the XXI Century:
Charlatans, Gurus and Pseudoscience (2013), Myths of Science: Millions of People Can be Wrong
(2012), Butterflies in the Brain: Forty Flutters about Science (2006), A Scientist at the Museum of
Modern Art (2011), and The Ugly Duckling Theorem (2013). In 2014, Luis was awarded the Jalisco
State Prize for Science, Technology, and Innovation, in the category of popular science writing.
Israel Llamas-Gonzalez studied Biology at Centro Universitario de Ciencias Biol6gico Agropecuarias,
Universidad de Guadalajara, Mexico, and took a course in Zoology at the Universidad de Costa Rica
in 2003. In 2005, Israel co-founded the sea turtle conservation project in Mayto, Jalisco, Mexico,
and in 2009 he founded the NGO Eco Mayto A.C. Currently, Israel is the Director of the Sea Turtle
Conservation Program in Mayto, and collaborates with the Environmental Ministry of Panama in
studying the Hawksbill Sea Turtle population in Coiba National Park, Panama. Photo by Alexander
Gaos.
Delia Karen E. Oceguera-Camacho graduated with a Marine Biology degree in 2002, and a Master’s
degree in 2004, from Universidad Autonoma de Baja California Sur (UABCS), Mexico. Karen worked
on a sea turtle research project with the Brazilian NGO TAMAR in the states of Bahia, Sergipe, and
Espiritu Santo, from January to April 2006, where she participated in the training of sea turtle monitoring
techniques, environmental education, and community integration. Karen founded and currently heads
the sea turtle protection and nesting conservation project in San Juan de Los Planes, Baja California Sur,
Mexico, which is celebrating its 14" year of conservation efforts. She is presently focusing on projects
which offer activities that improve the social and environmental aspects within local communities
through involving local community shareholders. In 2009, Karen joined the Mexican NGO Grupo
Tortuguero de las Californias A.C., where she coordinated multiple sea turtle nesting sites until 2013
when she transitioned into the role of Executive Director. Photo by K. Oceguera.
Alan Zavala-Norzagaray is a biologist who received his Ph.D. from the Universidad de Autonoma
de Sinaloa, Mexico. Alan received his B.S. from Universidad de Occidente (Mexico) and his M.S. in
Natural Resources and Environmental from the National Polytechnic Institute CIIDIR-Sinaloa, Mexico,
where he is currently a Research Professor, Coordinator of the Wildlife Program, and an adviser on
sea turtle foraging areas for Grupo Tortuguero de las Californias A.C. His current interests include the
ecology and conservation medicine of sea turtles in foraging areas, and the role that community groups
play in the conservation of sea turtles in northwest Mexico. Photo by A.A. Zavala-Norzagaray.
180 November 2019 | Volume 13 | Number 2 | e202
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Amphibian & Reptile Conservation
13(2) [General Section]: 181-202 (e204).
Diversity and conservation of terrestrial, freshwater, and
marine reptiles and amphibians in Saudi Arabia
‘Abdulhadi A. Aloufi, 7Zuhair S. Amr, 7Mohammad A. Abu Baker, and *Nashat Hamidan
‘Department of Biology, Taibah University, Al-Madinah Al-Munawwarah, KINGDOM OF SAUDI ARABIA *Department of Biology, Jordan
University of Science and Technology, Irbid, JORDAN *Department of Biology, The University of Jordan, Amman, JORDAN *Royal Society for the
Conservation of Nature, Amman, JORDAN
Abstract.—This review describes the diversity of the freshwater, marine, and terrestrial herpetofauna of the
Kingdom of Saudi Arabia that consists of 128 extant species and subspecies; 121 species and subspecies of
reptiles and seven species of amphibians according to current taxonomic systems. Four main categories of
threats affecting amphibians and reptiles were identified as habitat loss and degradation, water issues, human
disturbance and related activities, and legislation and public awareness; and supportive examples for each
category are provided. Key species that require urgent protection are: Chalcides levitoni, Platyceps insulanus,
Dasypeltis scabra, Hemidactylus alfarraji, Hemidactylus asirensis, Hemidactylus mindiae, Lytorhynchus
gasperetti, Pelomedusa barbata, Phoenicolacerta kulzeri ssp., Tropiocolotes wolfgangboehmei, and Varanus
yemenensis, due to their limited distribution, as well as Uromastyx aegyptia due to over-harvesting and trade.
According to the IUCN Red List, eight of these species are Data Deficient, four are Vulnerable, one Critically
Endangered, and one Near Threatened. The status of herpetofauna in Saudi Arabia is still far from being
completely understood. Nevertheless, the lack of formal conservation measures and low public concern makes
amphibians and reptiles extremely vulnerable in the near future.
Keywords. Anura, endemic, Sauria, Squamata, Testudines, threats
Citation: AloufiAA, Amr ZS, Abu Baker MA, Hamidan N. 2019. Diversity and conservation of terrestrial, freshwater, and marine reptiles and amphibians
in Saudi Arabia. Amphibian & Reptile Conservation 13(2) [General Section]: 181-202 (e204).
Copyright: © 2019 Aloufi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 1 February 2019; Accepted: 8 May 2019; Published: 6 December 2019
Introduction
Over the past century, several major publications on the
herpetofauna of Saudi Arabia have appeared (Schmidt
1941; Haas 1957; Haas and Werner 1969; Al-Wailly
and Al-Uthman 1971; Farag and Banaja 1980; Hillenius
and Gasperetti 1984; Balletto et al. 1985; Arnold 1986;
Al-Sadoon 1988, 1989; Gasperetti 1988; Al-Sadoon
et al. 1991; Leviton et al. 1992; Gasperetti et al. 1993;
Schatti and Gasperetti 1994; Al-Johany 1995). Many
additional publications have provided distributional
data, taxonomic reviews, descriptions of new species,
and new records (Hussein and Darwish 2001; Wilms and
Bohme 2007; Al-Sadoon 2010; Cunningham 2010; Al-
Shammari 2012; Smid et al. 2013, 2016; Al-J ohany et al.
2014; Aloufi and Amr 2015; Alshammari and Ibrahimm
2015; Al-Sadoon et al. 2016; Alshammari et al. 2017;
Algahtani 2018; Sindaco et al. 2018).
Some of these papers presented erroneous records that
should be interpreted with caution. For example, Schatti
and Gasperetti (1994) suggested that records of Zarentola
muritanica [sic] and Tarentola annularis by Farag and
Banaja (1980) should be referred to as Hemidactylus
flaviviridis. Also, the record of Mabuya quinquetaeniata
from date gardens north of Umluy by Farag and Banaja
(1980) certainly refers to Trachylepis brevicollis.
Dekinesh (1991) included records of Mabuya vittata,
Stenodactylus petrii, Trapelus savignyi, and Sphenops
sepsoides from Faid Hema, which later proved to be
misidentifications. Some of the contributions of Masood
(2012) and Masood and Asiry (2012) to the herpetofauna
of the Asir region comprise obvious misidentifications
and erroneous records that call for amendments. For
example, Masood and Asiry (2012) reported 7° annularis,
T. mauritanica, Tropiocolotes tripolitanus, and
Trachylepis vittata from the Asir region. Considering the
known distribution ranges of the aforementioned species
(e.g., see Schleich et al. 1996), these 7arentola records
must be doubted as well. Other doubtful records include
those of Stenodactylus sthenodactylus, Trapelus pallidus,
and Trapelus mutabillis (Masood and Asiry 2012).
The conservation status of the terrestrial reptiles
Correspondence. ! aaroufi@taibahu.edu.sa, ? amrz@just.edu.jo, > Ma.Abubaker@ju.edu.jo, *nashat@rscn.org.jo
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Ph
eo aBN,
HARRAT ~4
AL HARRAH “Ay
/
SAKAKAH e
HAFR ALBATIN,, . ‘
AL RIYA
ALLAT NAJD PLATEAU
AL SARAWAT
MOUNTAINS
of the Arabian Peninsula was assessed by Cox et al.
(2012). Some more recent works have focused on
individual countries. Carranza et al. (2018) discussed
the diversity, distribution, and conservation of the
reptiles of Oman, including records for 101 species of
terrestrial reptiles. The distribution of reptiles in Qatar
was presented by Cogalniceanu et al. (2014). Gardner
(2013) compiled distribution data for the amphibians
and reptiles of Oman and the United Arab Emirates.
Disi et al. (2014) gave a comprehensive account of
the diversity, conservation, and major threats for the
herpetofauna of Jordan.
Since the publications of Arnold (1986) on the lizards
of Arabia, Gasperetti (1988) on the snakes of Arabia,
and Leviton et al. (1992) on herpetofauna of the Middle
East, no updated lists covering Saudi Arabia have been
published. Many reptilian and amphibian species have
been subjected to critical reviews on the molecular and
morphological levels which resulted in the adoption of
new names. In addition to documenting and updating the
herpetofauna, based on current taxonomic understanding,
Amphib. Reptile Conserv.
Fig. 1. Map of Saudi Arabia showing main geographic landmarks (after Al-Nafie 2018).
3000 m
2000
1000
0
SAND
SABKHAH
EDGE —
PF as
VALLEY - =“
INTERNATIONAL == = = ==
§0 55 BORDERS
it is important to examine the impacts of continuous
drastic changes in habitats and some practices in Saudi
Arabia, as the reptiles and amphibians are being subjected
to several forms of threats that have caused declines in
some species.
In this study, the diversity, conservation status, and
major threats affecting the herpetofauna of Saudi Arabia
are identified, and an updated list, including the up-to-
date taxonomic names, is provided.
Materials and Methods
The Approach
Scientific names of the reptilian species mostly follow
Uetz et al. (2018). The taxonomic treatment of the genus
Phrynocephalus by Melnikov et al. (2014) was adopted.
The systematic position of Trapelus ruderatus (formerly
Trapelus persicus) was followed after Ananjeva et
al. (2013). For amphibians, the genera listed in the
Amphibian Species of the World (http://research.amnh.
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
Fig. 2. Ad Disah mountains, southwest Tabuk. Photo by S. Al Jathii.
org/vz/herpetology/amphibia/) were adopted. The
conservation status for species follow Cox et al. (2012).
Data on the threats affecting the reptiles and amphibians
were compiled from field observations mainly made
by the first author, A. Aloufi. Distributional limits
and localities were checked according to Sindaco and
Jereméenko (2008) for lizards, and Sindaco et al. (2013)
for snakes.
Geographical Setting
Saudi Arabia is a vast country occupying 2,026,213 km?
with diverse habitats that range from extreme arid and
basalt deserts, to mountain ranges and highlands, sand
and sandstone deserts, marine and freshwater ecosystems,
and numerous wadi systems and oases (Figs. 1-3).
Below is a general description of the geography of the
Kingdom of Saudi Arabia, including the Coastal Plains,
the Western Highlands, various plateaus, and sand dunes.
A. Coastal Plains
In Saudi Arabia, two strips of coastal plains extend along
the Red Sea and the Arabian Gulf.
The coastal plain of the Red Sea (Tihammah Plains)
lies between the Red Sea coast to the west and the western
highlands to the east. It is a narrow transitional area
between the Red Sea shelf and the high shelf mountains,
which becomes wider in the south; reaching up to 40
km wide near Jazan. To the north, it becomes narrower
until it disappears near 26°N latitude, south of Al Wajah.
With the exception of some parts near the northern tip
of the Red Sea, it 1s characterized by an abundance of
capes. The northern half of the plain is characterized
by a multitude of marine crusts, forming small marine
Amphib. Reptile Conserv.
clefts that deepen inland by water flow descending from
the coastal mountains such as Rabigh and Yanba’. The
southern half is characterized by the spread of salt flats
(Sabkha), especially along the coast, in addition to some
sandy settlements near the coast, and the spread of some
small black lava areas.
The coastal plain of the Arabian Gulf is limited to the
gulf coast to the east, and the As-Summan plateau to the
west. It is a flat plain largely covered by sand and salt flats
(Sabkha), especially near the coast and along its side.
This plain is devoid of wadi systems, with numerous sea
extensions and capes. The lowest point in Saudi Arabia
(24 m asl) lies within its southern part, near Al Homor
Sabkha.
B. Western Highlands
The western highlands consist of a mountain chain that
extends along the coast of the Gulf of Aqaba and the Red
Sea, stretching from Jordan to the north and reaching the
Republic of Yemen to the south. These mountains are a
refractive ladder-shaped formation, and its western slopes
descend precipitously towards the Red Sea, while inland
they descend gradually eastward. The altitude increases
towards the south, reaching as high as 3,015 m asl at the
mountain of Al-Sida, northwest of Abha. The western
highlands are divided into three main mountain series: Al
Sarawat mountains in the south, Al Hijaz mountains in
the middle, and Madyan mountains in the north (Fig. 2).
C. Plateaus
The hills or plateaus located to the east of the western
highlands cover large areas, and they generally descend
to the east and north-east.
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Diversity and conservation of reptiles and amphibians in Saudi Arabia
1. Western Plateaus
Najran and Asir plateaus are located to the east of the
Sarawat mountains (Figs. 3A—B), between the Kingdom's
borders and the Republic of Yemen to the south, and the
drainage system of Wadi Al-Dawasir valley to the north. In
this area of overlap they form a transitional area between the
Sarawat Mountains in the west and the Empty Quarter in
the east. Their altitudes range between 900 and 1,700 m asl.
The Hijaz Plateau is located to the east of the Hiyaz
Mountains, and is bounded by the Hijaz mountain to the
west, the Najd Plateau to the east, the plateaus of Najran
and Asir to the south, and the Hisma Plateau to the north.
Its southern part descends to the north and west, and its
northern part descends to the east and north-east. The
altitude reaches up to 1,200 m asl. Some of its stretches
include the black lava desert of Khaybar.
Hisam Plateau is located to the north-west of the Kingdom,
to the east of the mountains of Medyan, and to the west
and north-west of Tabuk. It is confined between the border
with Jordan to the north, and Hijaz Plateau to the south.
It descends eastwards, and ranges from 800—1,700 m asl.
Black lava deserts cover some of its southern parts (Fig. 2).
2. Central Plateaus
The Central Plateau is represented by An-Nafud or Najd
plateau, a large plateau located east of the Hijaz Plateau.
It is bordered to the west by Hijaz Plateau, to the east
by the sands of Ad-Dahna, to the south by the Wadi al-
Dawasir, and by the Greater An-Nafud to the north. The
An-Nafud near Tayma lies within the Arabian shield and
is called Najd High Plateau, while the eastern part, known
as Lower Najd Plateau, lies within the Arabian shelf. It
gradually descends towards the north-east in the north, to
the east in the middle section, and to the south-east in the
south, with an average altitude of 500—1,000 m asl. The
high plateau is characterized by igneous and metamorphic
rocks. In contrast, the lower Najd Plateau is characterized
by sand and rocky edges that extend from the north near
Zulfi to the center of the southwestern extremities of the
Empty Quarter, with a length of about 1,200 km.
3. Eastern Plateaus
The Eastern Plateaus are located in the eastern part of
the Kingdom, and the extent from its center to its north-
eastern edges is all within the Arabian shelf. The Eastern
Plateaus include four main plateaus.
As-Summan Plateau is located to the east of Najd
Plateau, where it is separated from Najd by Nofud Al
Dahna, and extends from the north to the south. It is
inserted between Ad-Dahna in the west, the coastal plains
of the Arabian Gulf in the east, and from Yibreen to the
Amphib. Reptile Conserv.
south of Wadi al-Sahba in the south. This plateau is wide
and semi-flat, descending slightly towards the north-east
and east, with altitudes ranging from 50-400 m asl.
Al Hajarh Plateau is located north-east of the Kingdom,
between As-Summan Plateau in the south and Al-Hammad
Plateau in the north. It is confined between the course of
Wadi Al-Batin in the south, the Valley of Aba Al-Qor in the
north, between the Nafud Al Dahna and the Greater Dahna
in the west, and the border of the Kingdom of Saudi Arabia
with Iraq in the east. A section of Al Hajarh also extends
north of the Greater An-Nafud towards the west, reaching
Al-Jawf, and it then descends towards the east and north-
east, with altitudes ranging from 400-600 m asl.
Al Hammad Plateau is located in the north-east of
the Kingdom, and it is confined between the Al Hajarh
plateau in the south, the borders of the Kingdom with
Iraq in the north, and between Harrat Al Harrah in the
west (Fig. 3C), and Al Wedyan Plateau in the east. It
descends to the northeast with altitudes ranging from
750-850 m asl.
Al Wedyan Plateau is located in the far northeast of the
country, bordering Al Hammad plateau in the east, and
it is considered as an extension of Al Hammad Plateau,
descending towards the north-east, with altitudes ranging
from 500—750 m asl. It is crossed by several wadi systems
that descend the Al Hammad plateau and drain rainwater
to Iraq during the rainy season.
D. Sand Dunes
The sand dunes cover a large proportion of the Kingdom's
area, about 677,715 km”, or about 33.8% of its total area.
The sands of the Empty Quarter, Greater Nafud (Fig.
3E-F), and Al Jaforah are the largest sandy seas, together
representing about 90% of the sand dunes in the country.
The sand dunes are concentrated in the eastern part of
the Kingdom, while small sandy gatherings occur in
the Arabian shield to the west, in addition to small and
scattered dunes along the Red Sea coast, formed from the
presence of sediment sources, watercourses, and wind.
Biogeographical regions of Saudi Arabia
Al-Nafie (2008) defined four main phytogeographical
regions in the Kingdom of Saudi Arabia (Fig. 4). The
Saharo-Arabian region occupies the greatest part of Saudi
Arabia, extending from the north, through central Arabia.
It includes As-Summan, Al Hammad, Al Hajarh, Al
Wedyan, and Najd plateaus, An-Nafud, Ad-Dahna, and
the Empty Quarter sand dunes. The Afromontane region
has mountains higher than 1,800 m asl, is dominated
by Juniperus procera and other evergreen shrubs, and
covers a narrow strip extending along Asir and Sarawat
mountains. The Sudanian region stretches over a narrow
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
Fig. 3. Landscapes and habitats in Saudi Arabia. (A) Juniperus procera forests in Raydah reserve. (B) Juniperus procera forests
in Asir mountains. (C) Harrat Al Harrah. (D) Harat Ewardh. (E) Sand dunes in the Greater Nofoud. (F) Sand dunes in the Empty
Quarter. (G) Elephant mountain in Al-’Ula. (H) Sharaan sand stones mountains in Al- Ula. Photos by K. Al Shamari (A), O.
Llewellyn (B), and A. Aloufi (C—H).
strip along the Red Sea coast as well as the Arabian Gulf
coast. Finally, the Sudanian-Zambian region surrounds
the Afromontane region, with overlaps with the Sudanian
region along the southwestern portions.
Results
Amphibians
Balletto et al. (1985) gave the most comprehensive
treatment to date of the amphibians of Arabia. Additional
distribution data were presented for central (Al-Johany
Amphib. Reptile Conserv.
2014) and southwestern Saudi Arabia (Al-Qahtani and
Al-Johany 2018), by Schatti and Gasperetti (1994) for
southwest Arabia, and by Alshammari and Ibnrahim
(2018) for Hai’l. Recent studies replaced Hyla savignyi
with the newly described taxon Ayla felixarabica
(Gvozik et al. 2010). Previous records of Bufotes viridis
are now considered as Bufotes boulengeri (see http://
research.amnh.org/vz/herpetology/amphibia/). In total,
seven species belonging to four families (Bufonidae,
Ranidae, Hylidae, and Dicroglossidae) are known from
the Kingdom of Saudi Arabia (Fig. 5, Table 1).
December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Table 1. List of amphibians and reptiles of Saudi Arabia, their IUCN conservation status, and levels of threats. IUCN status:
Critically Endangered (CR); Data Deficient (DD); Endangered (EN); Least Concern (LC); Near Threatened (NT); Not Evaluated
(NE); Vulnerable (VU). Threats: 1 = Deforestation, 2 = Destruction of the natural vegetation in the desert, 3 =Agricultural expansion,
4 = Overgrazing, 5 = Water extraction and climate change, 6 = Pollution and marine debris, 7 = Recreational activities and tourism,
8 = Direct persecution, 9 = Trade and commercial collection, 10 = Hunting and poaching. Levels of threats: L = Low, M = Medium,
H = High.
Tt Treats
ee
Ampbia TCrCUdT CrP PT dT PTC TCT YC
Framity Bufonidwe Sir SCT CCT PET PT TT
[ Bufnes boulengeri Laas 187) +f we | ne | | 1 |i] |] i]
[Dunaphsmus digerensis Parker, 53) | 1c | ne |_| | |[w] | | [2[ _
[Sopris er een“ [ue [we [PT
Amphib. Reptile Conserv. 186 December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
Table 1 (continued). List of amphibians and reptiles of Saudi Arabia, their IUCN conservation status, and levels of threats. IUCN
status: Critically Endangered (CR); Data Deficient (DD); Endangered (EN); Least Concern (LC); Near Threatened (NT); Not
Evaluated (NE); Vulnerable (VU). Threats: 1 = Deforestation, 2 = Destruction of the natural vegetation in the desert, 3 = Agricultural
expansion, 4 = Overgrazing, 5 = Water extraction and climate change, 6 = Pollution and marine debris, 7 = Recreational activities
and tourism, 8 = Direct persecution, 9 = Trade and commercial collection, 10 = Hunting and poaching. Levels of threats: L = Low,
M = Medium, H = High.
a 0
ee
tromaspmcegpia Forskal775) _|_vo | w | [a[ [al | [ep [ala
[ tromasy orata Heyden, 1827 _____| uc | 1c | |r] [xf | [et] |
FFamiyGekkonine Sid SSCS PE PT PT TT TC
[ Bunopus nbercdans Binford ira | ce | ie | | iz] |. 11.11
T Grtopodion scabram Weyden, 1827) | tc | 1c | || [z- | jefe] | _
Ee RT SD
Pepa ea es] I
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ia
a
Stenodactylus doriae (Blanford, 1874)
Stenodactylus grandiceps Haas, 1952
Stenodactylus slevini Haas, 1957
Stenodactylus yemenensis Arnold, 1980
Tropiocolotes nattereri Steindachner, 1901
Trigonodactylus arabicus (Haas, 1957)
Tropiocolotes wolfgangboehmei Wilms et al. 2010
ily
Acanthodactylus gongrorhynchatus Leviton and
Anderson, 1967
Family Phyllodactylidae
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Amphib. Reptile Conserv. 187 December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Table 1 (continued). List of amphibians and reptiles of Saudi Arabia, their IUCN conservation status, and levels of threats. IUCN
status: Critically Endangered (CR); Data Deficient (DD); Endangered (EN); Least Concern (LC); Near Threatened (NT); Not
Evaluated (NE); Vulnerable (VU). Threats: 1 = Deforestation, 2 = Destruction of the natural vegetation in the desert, 3 = Agricultural
expansion, 4 = Overgrazing, 5 = Water extraction and climate change, 6 = Pollution and marine debris, 7 = Recreational activities
and tourism, 8 = Direct persecution, 9 = Trade and commercial collection, 10 = Hunting and poaching. Levels of threats: L = Low,
M = Medium, H = High.
OS
ee
esdina arnold Sniaooeral,2018 | ve | ne | || f1i(24[,
T wesalina adramtana (Boulenger197) | 1¢ | uc | [cfz]| |] [et 7]
[ wesalina Bernoulli (Schenkel,190)___| Ne | ne | [t[x]| || [x] |]
[ Mesalina brevrostis Banford, 1874 | 1c | uc | [rfx]| |] [2] |]
Family Varanidae
Varanus griseus (Daudin, 1803)
Varanus yemenensis Bohme et al. 1989
Atractaspis engaddensis Haas, 1950
ily
Trachylepis septemtaeniatus (Reuss, 1834)
Family Trogonophidae
Diplometopon zarudnyi Nikolsky, 1907
Family Atractaspididae
Atractaspis andersonii Boulenger, 1905
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Aloufi et al.
Table 1 (continued). List of amphibians and reptiles of Saudi Arabia, their IUCN conservation status, and levels of threats. IUCN
status: Critically Endangered (CR); Data Deficient (DD); Endangered (EN); Least Concern (LC); Near Threatened (NT); Not
Evaluated (NE); Vulnerable (VU). Threats: 1 = Deforestation, 2 = Destruction of the natural vegetation in the desert, 3 = Agricultural
expansion, 4 = Overgrazing, 5 = Water extraction and climate change, 6 = Pollution and marine debris, 7 = Recreational activities
and tourism, 8 = Direct persecution, 9 = Trade and commercial collection, 10 = Hunting and poaching. Levels of threats: L = Low,
M = Medium, H = High.
a
ee
Platyceps saharicus Schatti and McCarthy, 2004 LC IF ecera i” kale (ietale elle Wi wile ole ell
Se ST
Calle
SITE ARES Sse Eee Seri
IME | ST eral a
itt tt tt tt et
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Echis coloratus Gunther, 1878
Pseudocerastes fieldi Schmidt, 1930
Reptiles
Twenty-one families in two orders, Testudines
(Cheloniidae, Dermochelyidae, Geoemydidae,
and Pelomedusidae) and Squamata (Agamidae,
Atractaspididae, Boidae, Chamaeleonidae, Colubridae,
Gekkonidae, Elapidae, Lacertidae, Leptotyphlopidae,
Phyllodactylidae, Psammophiidae, Scincidae,
Sphaerodactylidae, | Trogonophidae, Typhlopidae,
Varanidae, and Viperidae), including 55 genera and 121
Amphib. Reptile Conserv.
om
om
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pater
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[Halternnesa morgan (Mocquard, 1905) | VU
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species, have been recorded from Saudi Arabia (Table 1).
Testudines
Two species of freshwater turtles belonging to two
families have been recorded from Saudi Arabia:
Pelomedusa barbata (Pelomedusidae, Petzold et al.
2014) and Mauremys caspica (Geoemydidae, Gasperetti
et al. 1993; Vamberger et al. 2013). Algqahtani (2017)
published a detailed account on the status and distribution
189 December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Fig. 4. Phytogeographical regions of Saudi Arabia (after Al-Nafie 2008).
of P. subrufa (= Pelomedusa barbata) in Saudi Arabia.
Five species of marine turtles in two families
(Cheloniidae and Dermochelyidae) are known to occur
in the Red Sea (Ross 1985; Gasperetti et al. 1993; Al-
Merghani et al. 2000; Pilcher et al. 2014; Mancini
et al. 2015). The Green Turtle, Chelonia mydas, and
the Hawksbill Turtle, Eretmochelys imbricata, are
considered as the most common species in the Red Sea
(Fig. 6), where they feed and nest (PERSGA 2004).
Squamata
Family Chamaeleonidae
Hillenius and Gasperetti (1984) listed two taxa of
chameleons in Saudi Arabia: Chamaeleo calyptratus
calcarifer Peters 1871 and Chamaeleo chamaeleon
orientalis Parker 1938. Both species are confined to the
coastal mountains of the Red Sea, reaching up to 2,500
m asl.
Family Agamidae (Fig. 7)
Fifteen species belonging to six genera (Acanthocercus,
Phrynocephalus, Pseudotrapelus, Stellagama, Trapelus,
and Uromastyx) have been reported from Saudi Arabia.
Amphib. Reptile Conserv.
The status of species of the genus Phrynocephalus were
subjected to revisions based on the morphological and
genetic differences. Melnikov et al. (2014) differentiated
between the members of the Phrynocephalus arabicus
Anderson, 1984 complex. Their study revealed that Ph.
arabicus sensu Stricto is distributed in southern Arabia
(Yemen, Oman, southern Saudi Arabia), and Ph. nejdensis
in north-western Arabia (southern Jordan, northern and
central Saudi Arabia), while Ph. macropeltis is known in
the eastern coastal Arabia (eastern Saudi Arabia, United
Arab Emirates).
Rastegar-Pouyani (2000) published a controversial
opinion on the identity of Trapelus persicus. He stated
that the specific name “ruderatus’ (Olivier, 1804)
antedates “persicus’ (Blanford 1804), so the new
taxonomic combination is Trapelus ruderatus ruderatus
(Olivier, 1804) (= the former 7! p. persicus), and the
western subspecies 7’ p. fieldi has a new taxonomic
combination. Therefore, the name “persicus” is no
longer available and comes under the synonymy of
“ruderatus.” More recently, Ananjeva et al. (2013)
clarified the systematic position of 7rapelus ruderatus
in relation to 7? persicus, and for constancy and stability
of the taxonomy of this group, the International Code of
Zoological Nomenclature ruled that these two species
are separate. In addition, Pseudotrapelus aqabensis was
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
Ne Fe
T. Papenfuss.
Kw)
Fig. 5. Amphibians of Saudi Arabia. (A) Euphiyctis ehrenbergii. (B) Sclerophrys tihamica. Photos by
rd
7
BSG
us. (B) Stellagama stellio. (C) Phrynocephalus nejdensis. (D)
Te
Fig. 7. Agamids of Saudi Arabia. (A) Trapelus flavi
Pseudotrapelus sinaitus. Photos by A. Aloufi.
added recently to the herpetofauna of Saudi Arabia by = Cyrtopodion, Hemidactylus, _Pseudoceramodactylus,
Aloufi and Amr (2015) and Tamar et al. (2016b). Stenodactylus, Trigonodactylus, and Tropiocolotes), in-
cluding 18 species. The genus Stenodactylus was revised
Family Gekkonidae by Arnold (1980), Metallinou et al. (2012), and Nazarov
et al. (2018), and it now includes four species. Smid et al.
This family is represented by seven genera (Bunopus, (2013) revised the genus Hemidactylus. They considered
Amphib. Reptile Conserv. 191 December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Photos by A. Aloufi.
all previous records of Hemidactylus turcicus from Saudi
Arabia as Hemidactylus granosus. Recently Smid et al.
(2016) described two endemic species for Saudi Arabia:
Hemidactylus alfarraji from Najran area and Hemidacty-
lus asirensis from Asir Province. Hemidactylus mindiae
is a new addition to the geckos of Saudi Arabia (Aloufi
and Amr 2015). Therefore, the number of Hemidacty-
lus species known from Saudi Arabia is now eight. One
record of Hemidactylus sinaitus Boulenger, 1885 from
Seir Farasan Kebir should be considered with care (see
Sindaco et al. 2014). Tropiocolotes wolfgangboehmei
is known from a single locality in central Saudi Arabia
(Wilms et al. 2010).
Family Phyllodactylidae
This family is represented by one genus and one spe-
cies, Ptyodactylus hasselquistii. Recent molecular stud-
ies revealed that the genus Ptyodactylus in the Arabian
Peninsula consists of two species complexes for P. has-
selquistii, as eastern and western clades (Metallinou et
al. 2015). A new species, Ptyodactylus ananjevae, was
described from Al Mudawwarah, southern Jordan, very
close to Tabuk Province, so it is most likely to also occur
in Saudi Arabia (Nazarov et al. 2013).
Family Sphaerodactylidae
The Semaphore geckos of Saudi Arabia are represented
by five species. Their taxonomic status was discussed by
Arnold (2009). Recently, the status of Pristurus rupestris
was evaluated on a molecular basis, which showed that
P. rupestris 1s restricted to eastern Oman, while a western
clade, Pristurus sp. 1, 1s distributed from central coastal
Oman, through Yemen, Saudi Arabia, and north to
southern Jordan (Badiane et al. 2014). The northwestern
population in Saudi Arabia may be assigned as Pristurus
Amphib. Reptile Conserv.
Fig. 8. Scincids of Saudi Arabia. (A) E. urvlepis taeniolatus. (B) rachylepis brevicollis. (C) Chalcides ocellatus (D) Scincus scincus.
guweirensis, however, we still prefer to continue
referring to Pristurus sp. 1 as Pristurus rupestris until
further studies validate their separation.
Family Scincidae (Fig. 8)
Ten species of skinks have been reported from Saudi Ara-
bia, and they are represented by six genera (Ablepharus,
Chalcides, Eumeces, Eurylepis, Scincus, and Trachyl-
epis). The three species of the genus Scincus are strictly
sand-dwelling species. Chalcides levitoni is known from
only one locality in southwestern Saudi Arabia (Pasteur
1978). Panaspis wahlbergi was erroneously reported
from Saudi Arabia by Al-Jumaily (1984).
Family Lacertidae
Twenty species of lacertids occur in Saudi Arabia. They
belong to five genera (Acanthodactylus, Mesalina,
Ophisops, Philochortus, and Phoenicolacerta). Species
of the genus Acanthodactylus were extensively studied at
the molecular level (Tamar et al. 2016a), and constitute
the highest number of species, followed by species of
the genus Mesalina. Acanthodactylus tilburyi is known
only from Saudi Arabia and southern Jordan (Sindaco
and Jereméenko 2008). Among lizards of the genus
Mesalina, Sindaco et al. (2018) described Mesalina
arnoldi from southwestern Saudi Arabia and Yemen, and
Mesalina saudiarabica was described from Mahazat as-
Sayd, near Makkah (Smid et al. 2017). By now, Mesalina
brevirostris 1s known to be distributed in eastern Saudi
Arabia, while Mesalina bernoullii is known from north-
eastern Saudi Arabia (Smid et al. 2017). Al-Sadoon
et al. (2016) recorded Acanthodactylus orientalis and
Acanthodactylus robustus for the first time from Turaif
region. Phoenicolacerta kulzeri ssp. was recently
recorded from Al Konah, Tabuk (Aloufi and Amr 2015).
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
Family Trogonophidae (Fig. 9)
This family is represented by a single species in Saudi
Arabia. The Zarudny Worm Lizard, Diplometopon
zarudnyi, was reported from several localities mostly in
eastern Saudi Arabia.
Family Varanidae
Two species of the family Varanidae were reported
to occur in Saudi Arabia. Varanus griseus is widely
distributed across Saudi Arabia, while Varanus
yemenensis is confined to extreme southwestern Saudi OSEAN PAE EE
Arabia. Fig. 9. The Zarudnyi Worm Lizard, Diplometop
Photos by A. Aloufi.
ae py
on zarudnyi.
i
Fig. 10. Snakes of Saudi Arabia. (A) Eryx jayakari (B) Atractaspis engaddensis. (C) Echis coloratus. (D) Cerastes cerastes. (E)
Naja arabica. (F) Walterinnesia aegyptia. Photos by A. Al Salman (A-B, F), M. Al Sulimi (C), A. Aloufi (D), and M. Al Mesheni (E).
Amphib. Reptile Conserv. 193 December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Fig. 11. Snakes of Saudi Arabia. (A) Platyceps elagantissimus. (B) Telescopus dhara.
wo BS Oeeees
, vs a ss > 70% . $26
(C) Platyceps rhodarchis. (D) Psammophis
oS .
=
schokari. Photos by M. Al Sulimi (A), A. Al Salman (B-C), and A. Aloufi (D).
Family Leptotyphlopidae
Two species of the genus Myriopholis, Myriopholis
macrorhyncha and Myriopholis nursii, have been
reported from Saudi Arabia (Egan 2007).
Family Typhlopidae
This family is represented by a single species, /ndotyph-
lops braminus. This Asian species is widespread and has
become almost cosmopolitan in distribution. It 1s be-
lieved to have been introduced into Arabia through im-
ported plant pots (Egan 2007).
Family Atractaspididae (Fig. 10B)
Mole vipers in Saudi Arabia are exemplified by
two species: Atractaspis andersonii distributed in
southwestern Saudi Arabia, and Atractaspis engaddensis
in the northwestern and central parts of the country.
Family Boidae (Fig. 10A)
This family is represented by two species. Eryx jaculus
is known from eastern Saudi Arabia, while Eryx jayakari
is more common and widespread throughout the country.
Family Colubridae (Fig. 11)
Amphib. Reptile Conserv.
This family includes 13 species and _ subspecies
in six genera (Dasypeltis, Eirenis, Lytorhynchus,
Platyceps, Spalerosophis, and Telescopus). Three
species are confined to the extreme southwest of Saudi
Arabia (Platyceps insulanus, Dasypeltis scabra, and
Lytorhynchus gasperetti). Eirenis coronella coronella
is known from eastern Saudi Arabia, while FEirenis
coronella fennelli is known from the western part of
the country. Schatti and McCarthy (2004) confirmed
the occurrence of Platyceps saharicus in the Arabian
Peninsula. We came across a photographed specimen
of Rhynchocalamus melanocephalus from Al Konah,
near Tabuk and another one from Jabal Al Ward west of
Al-' Ula (data not shown). However, the validity of its
occurrence in Saudi Arabia requires further specimens.
Family Psammophiidae (Fig. 11D)
This family includes two species in two genera
(Psammophis and Rhagerhis). Both species are desert
adapted species with wide ranging distributions across
the Kingdom (Gasperetti 1988).
Family Elapidae (Fig. 10E and F)
Three species of terrestrial elapids belonging to two
genera (Naja and Walterinnesia) are known in Saudi
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Aloufi et al.
Arabia. Nilson and Rastegar-Pouyani (2007) considered
the eastern population of Walterinnesia as Walterinnesia
morgani and the western population as Walterinnesia
aegyptia. Naja arabica is distributed to the west of the
country.
Nine species of marine snakes belonging to the genus
Hydrophis have been reported from the waters of the
Arabian Gulf. The nomenclature of sea snakes in Table 1
follow Rezaie-Atagholipour et al. (2016).
Family Viperidae (Fig. 10C and D)
Six species in four genera (Bitis, Cerastes, Echis, and
Pseudocerastes) of vipers are known in Saudi Arabia.
Bitis arietans, Cerastes cerastes, and Echis borkini, are
confined to the southwest, while Pseudocerastes fieldi
occurs to the extreme north on the border with Jordan
within Harat Al Harah. Cerastes gasperetti is the most
common viper, especially in sandy areas.
Relict species
Pelomedusa barbata represents a relict population and is
known from southwestern Saudi Arabia (Gasperetti et al.
1993). This African species may have either migrated to
southern Arabia or originated in Arabia (Gasperetti et al.
1993; Vargas-Ramirez et al. 2016). The Caspian Turtle,
Mauremys caspica, reaches the most southeastern range
of its distribution around Al Qatif, Al Hufhuf, and Al
Ugayr (Gasperetti et al. 1993; Fritz et al. 2008), and these
populations are considered as relicts. The population
of Phoenicolacerta kulzeri ssp. from Al Konah, in the
northwest of Saudi Arabia, represents a relict in the
sandstone formation of Hisma (Aloufi and Amr 2015).
Endemic species
Seven species are strictly endemic to the Kingdom of
Saudi Arabia. 7ropiocolotes wolfgangboehmei is known
from one locality in the proximity of Ath-Thumamah,
central Saudi Arabia (Wilms et al. 2010). Chalcides
levitoni was recorded only from Khasawyah, near Jizan
(Pasteur 1978). Two snakes, Platyceps insulanus, known
only from Sarso Island, Farasan Archipelago (Mertens
1965; Masseti 2014), and Lytorhynchus gasperetti,
known from two localities in southwestern Saudi Arabia
(Leviton 1977), are considered as endemic species.
Recently, Hemidactylus alfarraji and Hemidactylus
asirensis were described from southwestern Saudi
Arabia (Smid et al. 2016), and Mesalina saudiarabica
was described from Mahazat as-Sayd (Smid et al. 2017).
Other species can be considered as endemic at the
level of the Arabian Peninsula. Four amphibians (Dut-
taphrynus dhufarensis, Euphlyctis ehrenbergii, Scleroph-
rys arabica, and Sclerophrys tihamica) are confined to
the Arabian Peninsula. Euphlyctis ehrenbergii is distrib-
uted in southwest Saudi Arabia, and the Riyadh locality
Amphib. Reptile Conserv.
may represent a release or escaped specimens from King
Saud University Campus (Al-Johany et al. 2014). Among
the reptiles, 20 species are restricted to the Arabian Pen-
insula excluding Socotra: Acanthocercus adramitanus,
Acanthocercus yemenensis, Acanthodactylus gongro-
rhynchatus, Acanthodactylus haasi, Atractaspis ander-
sonil, Chamaeleo calyptratus calcarifer, Echis borkini,
Mesalina arnoldi, Mesalina adramitana, Naja arabica,
Platyceps variabilis, Pristurus carteri, Pristurus mini-
mus, Pristurus popovi, Scincus hemprichii, Stenodacty-
lus arabicus, Stenodactylus yemenensis, Trapelus flavi-
maculatus, Trapelus jayakari, and Varanus yemenensis.
According to the distribution maps given by Sindaco
and Jereméenko (2008), 50 out of 97 lizard species
reported from the Arabian Peninsula are considered as
endemic to the Peninsula. Twenty-five species of these
reptile species are confined to the Arabian Hotspots
Areas as outlined by Mallon (2011).
Discussion
The Conservation Status of the Reptiles and
Amphibians of Saudi Arabia
Cox et al. (2012) revised the conservation status of the
reptiles of the Arabian Peninsula, excluding the marine
snakes and turtles. Among them, 101 species are listed
as Least Concern, eight are Data Deficient, four are
Vulnerable, one is Critically Endangered, and one 1s Near
Threatened (Table 1). However, some species listed as
Least Concern, such as Echis borkini, Bitis arietans, and
Naja arabica, are under threats due to human practices
and their status assessments require revision. Other
species that are listed under Data Deficient, such as
Acanthodactylus gongrorhynchatus, Chalcides levitoni,
Lytorhynchus gasperetti, Ophisops elbaensis, Platyceps
insulanus, Tropiocolotes wolfgangboehmei, and Varanus
yemenensis, have very restricted and very narrow ranges
of distribution and so they should be assigned with
conservation priorities.
Threats Affecting the Herpetofauna in Saudi Arabia
Four main categories of threats affect the amphibians and
reptiles of Saudi Arabia. Some of these threats are very
critical for a particular species, while other species may
be impacted by more than one type of threat that may
lead to population decline.
1. Habitat Loss and Degradation
The human population in Saudi Arabia has increased
more than seven-fold in the last 50 years, now reaching
up to about 33 million. This rapid growth resulted in the
expansion of cities and urban centers at the expense of basic
natural resources, especially wildlife and their habitats.
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Diversity and conservation of reptiles and amphibians in Saudi Arabia
Fig. 12. Habitat disturbance due to farming. (A) Fodder farms at Al Jawf. (B) Fodder farm in Tabuk. (C) Vegetable farms in Tabuk
area. (D) Farmland in Al-' Ula. Photos by A. Al Rabdi (B-C), and A. Aloufi (D).
Deforestation. It is estimated that forests and woodland
cover about 27,000 km? of Saudi Arabia. These
woodlands are mostly scattered along the Sarawat
mountain in the southwestern region and are dominated
by Juniperus procera. They have been subjected
to misuse through exhaustive wood cutting and
overgrazing activities, as well as uncontrolled forest
fire and urbanization (El-Juhany 2009). Dieback of J.
procera forests in the Raydah reserve of southwestern
Saudi Arabia was attributed to climate change and the
scarcity of rainfall, in addition to extensive farming
projects around the area (Fisher 1997).
The southwestern mountains are the home of
some rare, endemic, and perhaps endangered species
such as Acanthocercus adramitanus, Acanthocercus
yemenensis, Chalcides levitoni, Chamaeleo calyptratus
calcarifer, Euphlyctis ehrenbergii, — Lytorhynchus
gasperetti, and P. barbata. The conservation status
of these species should be assessed in relation to the
current state of vegetation cover.
Destruction of the natural vegetation in the desert.
As a result of agricultural expansion in the sand deserts
and wadi beds, the clearing of natural vegetation such
as Acacia raddiana, Acacia tortilis, Moringa peregrine,
Nitraria retusa, Ziziphus spina-christi, Retama reaetam,
and Haloxylon persicum, and other chenopods has
occurred. This clearance had direct effects on the lizards
that either use these plants for shading or feed on them.
Some species, such as TJrapelus persicus, take refuge
among Nitraria retusa shrubs. Uromastyx aegyptia is an
herbivorous lizard that feeds on a variety of desert plants
such as Pennisetum divisum and Stipagrostis plumose,
while Haloxylon salicornicum, Polygala_ erioptera,
Amphib. Reptile Conserv.
and Aerva javanica are consumed to a lesser extent
(Cunningham 2000).
Agricultural expansion. Over the past 30 years, large
parts of the deserts of Saudi Arabia were dedicated to
agricultural projects for the production of wheat, and were
converted recently for the production of green fodder and
other crops (Fig. 12). Most of these projects are located
around Tabuk, Tubarjal, Al Jawf, Hail, Buraydah, Sar,
Al Ula, and Wadi Al Dwasir, and were established since
the early 1980s. It is estimated that an area of 694,549
ha was cultivated with fodder, wheat, and other crops
in 2013. These projects were established in sandy areas
and around wadi courses, due to the availability of
groundwater. Alshammari and Ibrahim (2015) found
that the smallest numbers of reptiles were collected from
cultivated areas in Faid Hema, Ha'il region.
Much destruction of the natural habitats of sand-
dwelling species takes place due to the plowing and
construction of secondary roads in the desert. The
most heavily affected species include Acanthodactylus
schmidti, Cerastes gasperetti, Diplometopon zarudnyi,
Eryx jaculus, Lytorhynchus diadema, Phrynocephalus
nejdensis, Scincus hemprichii, Scincus mitranus, Scincus
scincus, Stenodactylus doriae, Varanus griseus, and
Uromastyx aegyptia.
Overgrazing. The nomadic lifestyle is still practiced in
many parts of Saudi Arabia. Sheep, goats, and camels are
among the domestic animals roaming the deserts and the
mountains during spring for grazing. This affects reptiles
in many ways, including direct disturbance, lowering
the vegetation cover, and actually abolishing entire plant
communities. Species such as Trapelus persicus are af-
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
fected by grazing and are displaced from their natural
habitats due to the year-round camel grazing on Nitraria
retusa shrubs.
2. Water Issues
Water extraction and climate change. Intensive farm-
ing in many parts of the Saudi deserts for the production
of wheat and fodder over the past 30 years has caused
drastic changes in the water table. This has led to a dra-
matic decrease in natural vegetation cover and drying of
natural ponds in the desert. The annual rainfall has shown
a significant decrease (47.8 mm per decade), with a rela-
tively high inter-annual variability, while temperatures
(maximum, mean, and minimum) have increased sig-
nificantly at rates of 0.71, 0.60, and 0.48 °C, respectively
(Almazroui et al. 2012). Eventually, the water re-charge
of aquifers will be affected for years to come. Accord-
ing to Alqahtani (2017), Pelomedusa barbata is facing
threats in southwestern Saudi Arabia as a result of rainfall
scarcity in recent years. In Al Hasa region, the number of
breeding sites of Mauremys caspica was reduced from
159 in the early 1970s to about 19 in 2009, due to de-
struction of natural springs and construction of cemented
canals, along with agricultural expansion (Aloufi 2009).
Pollution and marine debris. Cement dust pollution
has affected the Green Turtle, Chelonia mydas, in Ras
Baridi, reducing hatchling emergence success to only
40% due to the formation of hard domes above the nests
which prevent emergence and cause mortality (Pilcher
1999). As a result of urban sewage discharge in open
waters of the Red Sea, algal bloom formations have been
associated with fibropapillomatosis disease, which is
considered deadly to sea turtles (PERSGA/GEF 2004).
Marine pollution is also widely believed to affect other
sea turtles and snakes.
3. Human Disturbance and Related Activities
Recreational activities and tourism. Camping and
driving in the open areas are on the increase in Saudi
Arabia. Large vehicles and desert dirt bikes are widely
used for racing on the sand dunes. This will certainly
affect many sand-dwelling lizard and snake species, and
cause disturbance (Table 1). At the same time, many
shrubs and plants are destroyed during vehicle movement
across the terrain. Tourism causes disturbance to fragile
sensitive ecosystems, especially in places where relict or
endangered species exist.
Direct persecution. Reptiles in general, and snakes in
particular, are widely disliked animals. Many photos can
be found posted on social media which show snakes that
have been killed. Among them are venomous species,
Atractaspis andersonii, Atractaspis engaddensis,
Cerastes gasperetti, Echis coloratus, Naja arabica, and
Amphib. Reptile Conserv.
Walterinnesia aegyptia. However, non-venomous snakes,
such as Spalerosophis diadema cliffordii, Psammophis
schokari, and Platyceps rhodarchis, are also often
killed instantly even when they are encountered in the
wilderness. In Saudi Arabia, all forms of geckos are killed
since it is widely believed that they transmit leprosy.
Trade and commercial collection. We observed five
species of snakes that were traded in the animal markets
in Jeddah, Tabuk, Taif, and Al Madinah Al Monawarh:
Eryx jaculus, Naja arabica, Psammophis_ schokari,
Platyceps rhodorachis, and Spalerosophis diadema
cliffordii. These snakes were cramped in plastic bottles
and directly exposed to the sun. Lizards that were traded
in the animal markets included Chamaeleo chamaeleon,
Chamaeleo_ calyptratus, Scincus mitranus, Scincus
scincus, Uromastyx aegyptia, Uromastyx ornatus,
Varanus yemenensis, and Varanus griseus.
The Hawksbill Turtle, Evetmochelys imbricata, 1s
collected from the Red Sea and sold in animal markets
in Tabuk (Aloufi and Eid 2014). A less common item of
trade is the Western Caspian Turtle, Mauremys caspica,
but it can also be found in animal markets and pet shops
(Aloufi and Eid 2014) and sold in Riyadh and Al Hasa
Province. The population density of Pelomedusa barbata
is under stress and has decreased greatly over the last
few years in southwestern Saudi Arabia. However, it
is commonly taken from its freshwater habitats in the
southwest for trade (Alqahtani 2017).
The Spiny-tailed Lizard is sold for its meat, while
skinks (Scincus mitranus and Scincus scincus) are sold
as dried preparations that are prescribed in folk medicine
as aphrodisiacs. For animal exhibits and shows, snakes
such as Eryx jaculus, Naja arabica, and Psammophis
schokari are in demand. Most of these animals are sim-
ply disposed of after the shows, and it has been estimated
that over 100 Arabian cobras were killed in one season.
For teaching purposes, university students and high
schools purchase various amphibians, desert monitors,
and spiny-tailed lizards.
Hunting and pouching. The consumption of eggs
and meat of marine turtles has been reported in Saudi
Arabia (Miller 1989), however, this practice is not very
common. However, the major problem of hunting and
direct harvesting of the Egyptian Spiny-tailed Lizard,
Uromastyx aegyptia, is alarming. Thousands of these
animals are captured for human consumption and trade.
The locals relish both the meat and the eggs. Truckloads
of dead and slaughtered dabbs are posted on the hunter
internet sites as a sign of pride (Fig. 13). Gravid females
are in high demand due to their eggs. We counted over 17
females killed in one hunting trip, and females typically
lay 17-41 eggs in one clutch during May or June
(Bouskila 1984). This excessive harvest will certainly
affect the population of U. aegyptia, whereas large
numbers of females are killed in the eggs that are not
December 2019 | Volume 13 | Number 2 | e204
Diversity and conservation of reptiles and amphibians in Saudi Arabia
Fig. 13. The Egyptian Spiny-t
meat and eggs.
allowed to hatch. Both vitellogenic and oviductal eggs
were observed among the females that had been killed
(Fig. 13).
4. Legislative and Public Awareness
Enforcement. Although all wild animals in Saudi Arabia
are protected by law, enforcement is still far behind in
protecting the animals, and particularly reptiles. In fact,
the Spiny-tailed Lizard, U. aegyptia, is included among
the animals that are allowed to be hunted, together with
birds. The hunting season for the Spiny-tailed Lizard
is open from the beginning of August to the end of
September outside of the protected areas, with no bag
limit. This ambiguity in the number of allowed animals
has led to a massive scale of hunting and killing of
this vulnerable species. Until recently, the concept of
conserving diversity has remained obscure to many
decision makers in Saudi Arabia. The broad spectrum
of biological diversity in the country requires trained
individuals to reveal its importance for the country with
Amphib. Reptile Conserv.
ailed Lizard, Uromastyx aegyptia, 1s hunted and killed by the hundreds and sold either alive or for its
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respect to various aspects, including socio-economic,
ecotourism, scenic, and ethical perspectives.
Public awareness. As stated earlier, reptiles are disliked
by most of the locals, and surrounded by mystery and
superstitions. The general public attitude towards reptiles
is a mix of aversion and fear that stems from deep-rooted
traditional culture. Therefore, public awareness remains
one of the most important issues for introducing the
importance of reptiles to the general public; and public
awareness of the importance of conservation is a high
priority issue. The role of non-governmental organizations
is to introduce wildlife conservation to various sectors of
the community, mainly children and youngsters, as well
as to rally support from decision makers.
The environmental public awareness towards animals
in the Kingdom of Saudi Arabia remains limited, and
is almost totally lacking for reptiles. The availability of
books for providing scientific information to the public
or at the level of high school education remains very
limited. The lack of understanding in the general public is
clearly illustrated by social media being so full of videos
December 2019 | Volume 13 | Number 2 | e204
Aloufi et al.
and images of animal persecution and overhunting; with
expression of great pride in such actions.
Acknowledgments. We wish to thank Theodore J.
Papenfuss (Museum of Vertebrate Zoology, University
of California, USA), Othman Llewellyn and Khalaf Al
Shamari (Saudi Wildlife Authority), Ahmed Al Mansi
(Ministry of Environment, Water and Agriculture, Saudi
Arabia), Mohammed AI Mesheni (Oman), Abdusslam Al
Salman, Mushrief Al Sulimi, Abdulah. Al Rabadi, and
Saud Al Jathli (Saudi Arabia) for providing images for
some reptiles and the landscapes.
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Abdulhadi A. Aloufi is an Assistant Professor of Ecology, Faculty of Science, Taibah
University. Abdulhadi received his Ph.D. from King Saud University, Saudi Arabia, and his
(UAE), and Qatar.
Amphib. Reptile Conserv.
main interests are biodiversity and conservation. He has published about 20 articles and two
books on the biodiversity of the North Western region of Saudi Arabia and seabirds in Tabuk.
Abdulhadi has also written five books for children about animal welfare published by The
International Fund for Animal Welfare (IFAW).
Zuhair Amr is a Professor of Zoology and Animal Ecology in the Department of Biology,
Jordan University of Science and Technology, Jordan. Zuhair received his Ph.D. in Zoology
from the University of Rhode Island, Kingston, Rhode Island, USA. He has published over
150 papers and 10 books on various aspects of the ecology and systematics of mammals and
reptiles in Jordan, Lebanon, Syria, the Palestinian Territories, and Saudi Arabia. Zuhair serves
as the scientific authority for CITES in Jordan.
Mohammad Abu Baker is an Assistant Professor of Vertebrate Biology at The University of
Jordan. Mohammad received his Ph.D. in Biology from The University of Illinois, Chicago,
where he studied habitat selection and coexistence of African small mammals. He seeks to
understand local and regional factors that influence biodiversity and species distribution using
several empirical tools such as mark-recapture, camera trapping, foraging at experimental food
patches, wildlife tracking, and GIS. Thus far, Mohammad has over 40 publications on the
ecology, behavior, and natural history of mammals and reptiles in Jordan, Qatar, South Africa,
Egypt, and the USA. (Photo by Bruce Patterson).
Nashat Hamidan is the director of the Conservation and Monitoring Center at the Royal
Society for the Conservation of Nature, Jordan. Nashat received his Ph.D. from the University
of Bournemouth, United Kingdom. He has extensive experience in nature conservation and
reserves, and he has served in projects in Jordan, Saudi Arabia, Oman, United Arab Emirates
December 2019 | Volume 13 | Number 2 | e204
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 203-211 (e205).
Phylogenetic analysis of the Common Krait (Bungarus
caeruleus) in Pakistan based on mitochondrial and nuclear
protein coding genes
‘Muhammad Rizwan Ashraf, **Asif Nadeem, 7Eric Nelson Smith, ‘Maryam Javed,
2Utpal Smart, ‘Tahir Yaqub, ‘Abu Saeed Hashmi, and 7Panupong Thammachoti
‘Institute of Biochemistry and Biotechnology, University of Veterinary and Animal Sciences, Lahore, PAKISTAN *Amphibian and Reptile Diversity
Research Center and Department of Biology, University of Texas at Arlington, Arlington, Texas 76019, USA
Abstract.—Pakistan has more than 40 species of venomous snakes. One of them, the Common Krait
(Bungarus caeruleus), is responsible for most of the reported snake bites followed by Russel’s Viper, Saw-
scaled Viper, and Black Cobra. Molecular studies not only help in correctly identifying organisms but also in
finding the phylogenetic relationships and diversity among and between them. Morphological studies can be
supplemented with confirmatory molecular data to make them more authentic and accurate. This study is the
first to characterize the genetic diversity and phylogenetic relationships of Common Kraits from Pakistan,
which will help in developing effective strategies for managing snake bites through effective antivenom
development. Tail tip biopsies of 25 Common Kraits were collected from different cities in Pakistan. The whole
DNA was extracted. Four mitochondrial (ND4, Cytochrome b, 12S rRNA, and 16S rRNA) and three nuclear
protein coding (C-mos, RAG-1, and NT3) gene fragments were amplified using specific PCR primers. The
amplified DNA was sequenced by Sanger di-deoxy sequencing. Forward and reverse sequences were cleaned
and contiged using Sequencher 5.0 software. DNA data were aligned and concatenated using MEGA 6.0 and
SequenceMatrix software, respectively. Partition Finder software was used for obtaining the best partitioning
scheme and evolutionary models. Concatenated maximum likelihood and Bayesian phylogenetic trees were
constructed using RaxML and MrBayes software. The same alignments were used to perform DNA polymorphism
analysis using DnaSP 5.0 software. A percent identity matrix was created for all sequences using the online
bioinformatics tool, MUSCLE. Homology was presented in tabular form, showing the similarity among different
species of genus Bungarus. All Bungarus species were differentiated into four groups. Common Krait (B.
caeruleus) from Pakistan showed close relationships with B. sindanus and B. ceylonicus, as one monophyletic
group. The first clade included B. candidus (Indonesia, Thailand, Vietnam, and Laos), B. multicinctus (China,
Taiwan, and Burma), and B. niger (Nepal). The second clade included B. sindanus and B. caeruleus (Pakistan),
and B. ceylonicus (Sri Lanka). The third clade included B. fasciatus (Thailand and Indonesia), while the fourth
clade included B. bungroides (China) and B. flaviceps (Malaysia and Indonesia). This study traces the diversity
and phylogenetic relationships of the Pakistani elapid, Common Krait, showing the considerable inter- and
intra-specific variations from different geographical regions of the world.
Keywords. Asia, Elapidae, PCR, polymorphism, Serpentes, venomous snakes
Citation: Ashraf MR, Nadeem A, Smith EN, Javed M, Smart U, Yaqub T, Hashmi AS, Thammachoti P. 2019. Phylogenetic analysis of the Common
Krait (Bungarus caeruleus) in Pakistan based on mitochondrial and nuclear protein coding genes. Amphibian & Reptile Conservation 13(2) [General
Section]: 203-211 (e205).
Copyright: © 2019 Ashraf et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 25 January 2019; Accepted: 24 September 2019; Published: 17 December 2019
Introduction
Snakes are legless carnivorous reptiles of suborder
Serpentes, and their lack of eyelids and external ears
distinguish them from legless lizards (Reeder et al. 2015).
Except Antarctica and some other large islands, like
Ireland, Iceland, Greenland, the Hawaiian archipelago,
Correspondence. * asifnadeem@uvas.edu.pk
Amphib. Reptile Conserv.
and New Zealand islands, snakes are found everywhere
in the world (Roland 1994). South Asia is the region
most affected with venomous snake bites. For example,
the World Health Organization reports 35,000 to 50,000
deaths annually in India (Chippaux 1998; Pyron et al.
2013), and Pakistan reports 40,000 snake bites every
year that result in 8,200 fatalities (Pyron et al. 2013).
December 2019 | Volume 13 | Number 2 | e205
Bungarus caeruleus in Pakistan
=a
Sie Mth ee A ipl Bieareeeed,
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AFGHANISTAN
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fe
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Kunduz
aaa (STINK IAN
a) So
| :
UMEDECONTIOL)
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. (Tt
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ero
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Fig. 1. Sample collection sites in Pakistan for Common Krait (Bungarus caeruleus).
Venomous snakes in Southeast Asia belong to families
Elapidae (cobras and kraits) and Viperidae (typical vipers
and pit vipers). A study of hospital-admitted snakebite
cases in Pakistan revealed less than 5% neurotoxic
snakebites, and the rest were viper bites (Nisar et al. 2009).
Kraits, genus Bungarus, are identified by alternating
black and white cross-bands across the body, and are found
in all South Asian countries except the Philippines. Members
of genus Bungarus are moderate to large sized elapids
distributed in Pakistan and eastward through southern Asia
to Indonesia (Smith 1943). Currently, 12 species of kraits are
recognized (Yulin et al. 2018), including three in Pakistan.
In Pakistan, Common Kraits (Bungarus caeruleus) are
reported throughout Punjab, Khyber Pakhtoonkhwa
(KPK), Azad Kashmir, Sindh, and Southern Balochistan.
Common in the Indus valley, this 1s the only species of
kraits found in Rawalpindi and Islamabad (Khan 2002a;
Oh et al. 2019). Sindhi Krait (B. sindanus) is prevalent in
Tharparkar, Bahawalnagar, and Bahawalpur. Northern
Punjab Krait (B. razai) is reported from Mianwali (Khan
2002b). Determining the relationships among the members
of Elapidae can help in understanding their distribution and
diversity. Many studies have focused on the evolutionary
relationships of kraits.
Before the widespread use of DNA sequencing,
systematics and taxonomy were used to infer phylogenies
among species in order to explain their relationships.
Now many fields in biology are using phylogenies for a
wide variety of purposes, such as examining paralogous
relationships, population histories, dynamics of pathogens
with respect to their evolution and epidemiology (Zhou
et al. 2018; Blanquart 2019), the ontogeny of body
cells during development, and the differentiation of
tumors (Kester and van Oudenaarden 2018). Variations
in nucleotide sequences can construct phylogenies for
Amphib. Reptile Conserv.
inferring relationships among the compared sequences.
The topology of phylogeny gives some estimates about
the mutation rates, time-scales of evolutionary events,
and prehistoric movement among different geographical
regions (Soroka and Burzyfski 2018). Phylogenetics
shows relationships among organisms and genes
(Friberg et al. 2019), and can give a clearer picture of
the biodiversity, biogeography, and evolution of many
characters in related groups (Pilfold et al. 2019; Grismer
and Davis 2018; Silva et al. 2019).
The use of mitochondrial DNA data for studying
animal evolution has become a powerful tool in
the last decade. Molecular biology has helped in
these mitochondrial DNA studies to give insights
into population structure, gene flow, hybridization,
biogeography, and phylogenetics (Chandrasekaran et
al. 2019; Soroka and Burzynski 2018). Evolutionary
studies give comparisons of mitochondrial genome
organization and function while molecular studies
help to improve these evolutionary studies (Ng et al.
2019). Nuclear encoded genes seem to be a strong
source of phylogenetic information. They can be
more useful for showing the divergence of those
genes whose multiple substitutions may obscure
clear phylogenetic signals.
This is the first study from Pakistan focusing on
genetic characterization, biodiversity, and molecular
phylogenetics of the Common Krait (Bungarus
caeruleus).
Materials and Methods
A collection of 25 Common Kraits (Bungarus caeruleus)
was obtained from reptile breeders in different cities in
Pakistan (see Fig. 1, Table 1). Scalation patterns and
December 2019 | Volume 13 | Number 2 | e205
Ashraf et al.
Table 1. Common Krait (Bungarus caeruleus) samples used in this study, and their location information.
Sample ID
BC-1
BC-2
BC-3
BC-4
BC-5
BC-6
BC-7
BC-8
BC-9
BC-10
BC-11
BC-12
BC-13
BC-14
BC-15
BC-16
BC-17
BC-18
BC-19
BC-20
BC-21
BC-22
BC-23
BC-24
BC-25
tail tip biopsies were obtained from each specimen.
After DNA extraction (Sambrook and Russel 2001),
the Polymerase Chain Reaction (PCR) primers of
representative mitochondrial genes (ND4, Cytochrome
b, 12S rRNA, and 16S rRNA) and nuclear genes
Locality
Jallo Park, Lahore, Punjab, Pakistan
Balochanwali, Bahawalpur, Punjab, Pakistan
Qila Ram Qaur, Hafiz Abad, Punjab, Pakistan
Yazman Housing Society, Yazman, Punjab, Pakistan
Changa Manga Forest, Kasur, Punjab, Pakistan
Lal Suhanra National Park, Bahawalpur, Punjab, Pakistan
Rahim Yar Khan Zoo, Rahim Yar Khan, Punjab, Pakistan
Chak Risalwala, Faisalabad, Punjab, Pakistan
Qila Ram Qaur, Hafizabad, Punjab, Pakistan
New City Housing Society, Jaranwala, Punjab, Pakistan
Chak 126 GB Pind Janjua, Jaranwala, Punjab, Pakistan
Rahim Yar Khan Zoo, Rahim Yar Khan, Punjab, Pakistan
Yazman Housing Scheme, Yazman, Punjab, Pakistan
Ayub National Park, Jehlam Road, Punjab, Pakistan
Tibbi Balochan, Sadiqabad, Punjab, Pakistan
Maraghzar Colony, Lahore, Punjab, Pakistan
Lahore Zoo, Punjab, Pakistan
Lahore Zoo, Punjab, Pakistan
Raza Garden Phase 1, Sargodha, Punjab, Pakistan
Pir wala, Jhang, Punjab, Pakistan
Noor Garden, Okara, Punjab, Pakistan
Chenab Park, Multan, Punjab, Pakistan
Kalarwala, Chiniot, Punjab, Pakistan
Qadir Abad Tiba, Sadiqabad, Punjab, Pakistan
Chenab Park, Gujranwala, Punjab, Pakistan
Latitude
31°34'17.29"N
29°28'56.90"N
32°4'57.12"N
29°7'3.00"N
31°4'54.19"N
29°19'1.36"N
28°24'14.30"N
31°22'4.90"N
32°4'57.12"N
31°19'16.60"N
31°21'38.48"N
28°24'14.30"N
29°6'54.39"N
33°34'19.00"N
28°16'35.01"N
31°30'8.71"N
31°33'23.78"N
31°33'23.78"N
32°2'51.23"N
31°1'42.61"N
30°48'48.38"N
30°4'29.90"N
31°28'26.21"N
28°16'54.33"N
30°4'29.90"N
Longitude
74°28'36.78"E
71°59'41.86"E
73°40'49.02"E
71°45'6.73"E
73°59'53.49"E
71°54'16.43"E
70°15'32.63°E
73°1'24.80"E
73°40'49.02"E
73°23'21.44"E
73°25'28.74"E
70°15'32,63"E
71°45'17.40"E
73°4'59.00"E
70°8'6.58"E
74°14'55.48"E
74°19'33.73"E
74°19'33.73"E
72°37'31.68"E
72°16'45.51"E
73°28'38.33"E
71°18'51.93"E
72°33'56A1"E
70°7'45.48"E
71°18'51.93"E
(C-mos, RAGI, and NT3) from previous studies were
used for the amplification of selected regions through
PCR (see Table 2). After amplification, amplicons were
sequenced bi-directionally by Big DyeTM Terminator
on an ABI 3130XL Genetic analyzer. Forward and
Table 2. Mitochondrial and nuclear protein coding gene primers for Common Krait (Bungarus caeruleus).
Sr. No
1
Amphib. Reptile Conserv. 205
Gene Name Primer Sequence Source
Cyt.b 5'-TGACTTGAARAACCAYCGTTG-3' Palumbi 1996
5'-TGAGAAGTTTTCYGGGTCRTT-3' Parkinson et al. 2002
16S rRNA 5’-CGCCTGTTTAYCAAAAACAT-3 Vences et al. 2005
5’-CCGGTCTGAACTCAGATCACGT-3’ Vences et al. 2005
12S rRNA 5’>GTACACTTACCTTGTTACGACTT 3’ Knight and Mindell 1993
5’ AAACTGGGATTAGATACCCCACTAT3?’ Knight and Mindell 1993
ND4 5’-CATTACTTTTACTTGGATTTGCACCA-3’ Arevalo 1994
5’-CACCTATGACTACCAAAAGCTCATGTAAGC-3’ Arevalo 1994
RAG-1 5’ AGCTGCAGYCARTAYCAYAARATGTA3’ Chiari et al. 2004
S’AACTCAGCTGCATTKCCAATRTCA3’ Chiari et al. 2004
NT3 S’ATATTTCTGGCTTTTCTCTGTGGC3’ Townsend et al. 2008
5’GCGTTTCATAAAAATATTGTTTGACC3’ Townsend et al. 2008
C-mos 5' CATGGACTGGGATCAGTTATG 3' Lawson et al. 2005
5'CCTTGGGTGTGATTTTCTCACCT 3' Lawson et al. 2005
December 2019 | Volume 13 | Number 2 | e205
Bungarus caeruleus in Pakistan
100
Bungarus_multicinetus Bm] China
100
Bungarus_moulticinetes_ Bm9204 Taiwan
100 Bungarus_candidus_UR_BT1_Thailand
100
- Bungarvs_candidus Feba_ Indonesia
4 T
3 Bungarus_candidus FMNH_235260 Laos
a8
Bungarus_candidus Emnam Vietnam
OK)
Bungarus_ multicineis CAS 221526 Burma
100 Bungarus_niger Bniz Nepal
Bungarus_sindanus Bein] Palostan
100 Bungarus_cevlonicus_F8 135
oo B caerulevs_4 Yarman Mandi Ponjab Palastan
100
B_caeruleus_6 Baharalpur_Ponjab_Palastan
rh
Bcaerilens_ 1] Jaramrala_Ponjab_Palastan
5
B caerclevs_12 Rahim Yar Khan Ponjab Palostan
On
Bungarus_caervlens_UK_H? Palastan
Bungarus_fasciatus_URB24 Java_Indonesia
100
Bungarus_ fasciatus BiasT Thailani
Bungarus_bungaroides KIV9SR0196 China
Bungarvs_flaviceps_ JAM0946 Whlaysia Perak
100
Bungarus_flaviceps_MNHN_Indonesia_ Sumatra
Naja_naja_8 Thatta Thatta District Sind Palastan
0.2
Fig. 2. Mitochondrial and nuclear genes (ND4, Cyt. b, COI, 12S rRNA, 16S rRNA, C-mos, RAG-1, NT3, and BDNF) based
Maximum Likelihood phylogeny for Common Krait (Bungarus caeruleus).
reverse sequences were assembled through Sequencher
5.0 software. The resulting contigs (sequences) were
given specific identities. These contigs were then aligned
with other reported sequences obtained from the NCBI
database through MEGA (v 6.0, Tamura et al. 2013)
using the ClustalW tool for further data analyses. The
nucleotide data for each gene were concatenated using
SequenceMatrix (v1.7.8, Vaidya et al. 2011) software.
The concatenated data were partitioned through
PartitionFinder (v1.1.1, Lanfear et al. 2012) to give
the best partition scheme and evolutionary models for
phylogenetic analyses.
Two types of phylogenetic analyses, 1.e., Maximum
Likelihood (ML) and Bayesian inference (BI), were
performed through RaxML (v8.0, Stamatakis 2014)
and MrBayes (v3.2, Ronquist and Huelsenbeck 2012)
software. The resulting phylogenetic trees were
visualized and saved using Figtree (v1.4.3, http://tree.
bio.ed.ac.uk/software/figtree/) software. DnaSP (v5.0,
Librado and Rozas 2009) was used for analyzing
polymorphic sites and DNA polymorphism, to determine
the variation and genetic biodiversity in Common Krait
(Bungarus caeruleus) in relation to other species of the
genus Bungarus. Percent identity matrices were also
constructed by comparing different species of every
snake genus using online tool MUSCLE (available from
the European Molecular Biology Laboratory, https://
www.ebi.ac.uk/Tools/msa/muscle/).
Results
DnaSP software was used for analyzing the polymorphism
of the mitochondrial and nuclear genes as shown in Table
3. The ribosomal RNA coding genes showed the least
Amphib. Reptile Conserv.
variation, with lower numbers of variable sites, mutations,
and parsimony informative sites. The polymorphism
data show the variations in different mitochondrial and
nuclear genes with their conservation among Common
Krait and other species of genus Bungarus. In addition,
no significant variations were found among Common
Kraits from different cities in Pakistan.
The online MUSCLE tool was used to find relationships
among Bungarus species on the basis of homology in the
mitochondrial and nuclear genes (Table 4). This table
shows the conservation patterns in mitochondrial and
nuclear protein coding genes of various Bungarus species.
Phylogenetic analysis of Common Krait (Bungarus
caeruleus) from Pakistan was conducted using
mitochondrial and nuclear protein coding genes. In
this study, Black Cobra (Naja naja) from Thatta Sindh
was used as the outgroup for constructing maximum
likelihood and Bayesian phylogenies. The best partition
scheme and evolutionary models were used to infer the
phylogenetic relationships of Common Krait in Pakistan
with other members of genus Bungarus around the
world. Concatenated Maximum likelihood and Bayesian
Inference results gave very similar phylogenies (Figs.
2-3). All Bungarus species were divided into four main
clades. The first clade included B. candidus (Indonesia,
Thailand, Vietnam, and Laos), B. multicinctus (China,
Taiwan, and Burma), and B. niger (Nepal). The second
clade included B. sindanus and B. caeruleus (Pakistan),
and B. ceylonicus (Sri Lanka). The third clade included
B. fasciatus (Thailand and Indonesia), while the fourth
clade included B. bungroides (China) and B. flaviceps
(Malaysia and Indonesia). The first and second clades
showed a sister clade relationship with strong support
(ML BS = 100, BI PP = 1). Bungarus candidus and
December 2019 | Volume 13 | Number 2 | e205
Ashraf et al.
1
B caervlevs 4 Yaemnan Mandi Punjab Palastan
B_caervleus_6 Baharalpur_Penjab Palastan
0.6108
B_eaervlevs_1]_ Jaramvala_Ponjab Pelastan
0.9893 “a. : !
1 B ecaerulevs_12 Rahim Yar Khan Ponjab Palastan
Bungarus_caervlevs UK_H? Palastan
Bungarus_ceylonicus_RS 155
Bungarvs_sindanus Bein] Palastan
Bungares_candidus Beba_ Indonesia
0.9995 7 : ,
Bungarus_candidus UFR_BT1 Thailand
0.8295
Bungarus_candidus_ Bmnam Vietnam
0.9997
1+ Bungarus_candidus FMONH 253260 Lane
Bungarus multicinetus Bm] China
0.900]
Bungarus_multicinetes_Bm S204 Taiwan
0.998
Bungarvs_multicincs CAS 221326 Burma
0.9902 had ae
Bungarus_nizer Bniz Nepal
Bungarvus_fasciatus_BiasT Thailand
Bungarus_fasciatus_UR B24 Javea_Indonesia
Bungarus_bungarcides RIZ9SR0186 China
0.9475
0.9649
Bungarus_flaviceps_MMNHM_Indonesia_ Sumatra
Naja_naja_§ Thatta _Thatta_District_Sind_Palastan
0.08
Bungarus_flavieeps JAMI946 Malaysia Perak
Fig. 3. Mitochondrial and nuclear genes (ND4, Cyt b, COI, 12S rRNA, 16S rRNA, C-mos, RAG-1, and NT3) Bayesian phylogeny
for Common Krait (Bungarus caeruleus).
B. multicinctus probably diverged as separate species
only recently. Bungarus candidus, B. multicinctus, and
B. niger showed highly supported sister relationships
with a complex pattern of divergence (BI PP = 1.0
ML BS = 90). In the second clade B. sindanus and B.
caeruleus have been reported from Pakistan, thus they
are sympatric species, while B. ceylonicus (from Sri
Lanka) also showed a significant difference with strong
support through Maximum likelihood and Bayesian
inference phylogenies (PP = 1.0 and BS = 100). Pyron et
al. (2012) also revealed the same relationships between
B. caeruleus, B. sindanus, and B. ceylonicus.
In addition to the molecular data obtained, examination
of the 25 B. caeruleus specimens showed varying numbers
of ventral scales (207—218), 15 rows of mid-body scales,
and average numbers of subcaudals of 41-47.
Discussion
Elapids comprise 300 of the 2,500 known species
of snakes (Leviton et al. 2018). The Southern Asian
elapids include cobras (Naja and Ophiophagus), kraits
(Bungarus), long-glanded snakes (Maticora), and Asian
coral snakes (Calliophis) [Sanz et al. 2019]. The uncertain
phylogenetics of elapids has been a major factor for the
varying numbers of identified species of elapids in the
past (Mirtschin et al. 2017).
This study aimed to characterize the genetic
biodiversity and phylogenetic relationships of Common
Krait (Bungarus caeruleus) as there is a great deal of
unpublished data on this species. Here, mitochondrial
and nuclear protein coding genes were used to construct
the phylogeny of Common Krait from Pakistan along
with some morphological characterization. One variable
character is the number of ventral scales that ranges from
207-218 among the 25 specimens in this study. Khan
(1985) wrote a note on the taxonomic status of Common
Krait and Sindh Krait (B. sindanus), and by comparing
46 specimens, Khan noted an almost similar range of
207-218 ventral scales. The B. caeruleus in this study
had 15 rows of mid-body scales which is the same as
described by Khan (1985). Bungarus caeruleus and B.
Table 3. Polymorphism in mitochondrial and nuclear protein coding genes of Common Krait (Bungarus caeruleus).
Parameters ND4 Cytochrome b
Total number of sites 619 702
Variable number of sites 302 325
Number of mutations 302 202
Singleton variable sites 43 51
Parsimony informative sites 196 151
Segregating sites 159 151
Synonymous changes 176 156
Number of haplotypes 17 16
Haplotype diversity 0.866 0.615
Nucleotide diversity 0.08243 0.09528
Amphib. Reptile Conserv.
128 rRNA 16S rRNA C-mos RAG-1 NT3
650 520 586 802 425
270 19] 419 665 325
63 47 12 20 32
20 26 09 19 03
43 21 03 01 28
00 00 12 19 31
00 00 06 03 23
08 10 04 03 05
0.686 0.521 0.333 0.145 0.754
0.03617 0.03451 0.00288 0.00226 0.03389
207 December 2019 | Volume 13 | Number 2 | e205
Bungarus caeruleus in Pakistan
Table 4. Percent homology of mitochondrial and nuclear genes for Common Krait (Bungarus caeruleus) from Pakistan among
various Bungarus species and countries, sorted by decreasing Cytb homology. The asterisk (*) indicates the sequence from this
study, all others are based on GenBank sequences.
Homology percentages of nine representative genes
Species Country Cytb ND4 128
B. caeruleus* Pakistan 100 100 100
B. caeruleus Pakistan 99.84 99.51 100
B. ceylonicus NA 89.21 87.46
B. candidus Indonesia 89.19 84.53
B. niger Nepal 86.31 84.36
B. sindanus Pakistan 86.31 85.5
B. candidus Thailand 85.35 83.88
B. multicinctus Burma 85.19 84.34
B. multicinctus China 85.19 85.18
B. candidus Vietnam 85.19 85.67
B. multicinctus Taiwan 85.02 85.5
B. fasciatus Thailand 83.74 83.55
B. fasciatus Indonesia 83.57 83.39
sindanus had 15 and 17 rows of mid-body scales, with
the central larger row being hexagonal and white in color.
Boulenger (1897) also observed 15 rows of mid-body
scales in Indo-Pakistan Common Krait while 17 mid-
body scale rows were reported in B. sindanus from Indus
Basin. The average number of sub-caudals observed here
is 41-47 which is within the range observed by Khan
(1985): 40-54 in males and 30—54 in females. Boulenger
(1897) reported small eyes with round pupil which is
similar to those observed in this study.
There are also reports about the distribution of B.
caeruleus in Indo-Pakistan subcontinent. Eastward
it is found in Assam and Bengal (Jamal et al. 2018;
Ganesh and Vogel 2018); westward to the Pakistan-
Iran Border; Shockley (1949) and Kral (1969) reported
it in Afghanistan; Smith (1943) reported it southward
in Peninsular India and the Andaman Islands; and de
Silva (1981) also reported it in Sri Lanka. This study is
one attempt to infer the phylogenetics of B. caeruleus
in Pakistan, but suggests more studies from the above-
mentioned parts of the B. caeruleus distribution are
needed, as there are almost no studies from other parts of
of the Indo-Pakistan subcontinent on the phylogenetics
of the Common Krait B. caeruleus.
Determining the relationships among the members
of Elapidae can help in understanding the distribution
and diversity of elapids. Many studies have focused
on evolutionary relationships of elapids, and this study
examined the molecular phylogenetics of B. caeruleus
from Pakistan. The second clade (Figs. 2—3) includes B.
sindanus and B. caeruleus (Pakistan), and B. ceylonicus
(Sri Lanka). Bungarus sindanus and B. caeruleus are
sympatric species, while B. ceylonicus also showed a
significant difference with strong support through the
Maximum likelihood and Bayesian inference phylogenies
Amphib. Reptile Conserv.
93.68
90.57
i Li 2)
90.79
91.38
16S COI C-mos RAG-1 NT3 BDNF
100 100
100 99.99
96.62 100 99.4
95.08
85.65
90.09 86.11
91.91
95.5 85.03 99.38 99 62 96.63 99.76
(PP= 1.0 and BS = 100). Pyron et al. (2012) also revealed
the same relationships between B. caeruleus, B. sindanus,
and B. ceylonicus. They presented a large-scale phylogeny
of squamate reptiles for future comparative studies, and
a revised classification of squamates at the family and
subfamily levels so that taxonomy might be brought
in a line with data from the new phylogenetic studies.
Their phylogeny shows the same relationship (ML BS =
100, BI = 1) between B. caeruleus, B. sindanus, and B.
ceylonicus as is shown in this study through Maximum
Likelihood and Bayesian phylogenies.
Conclusions
Most of the currently recognized krait species
(genus Bungarus) are poorly understood. This study
characterized the genetic biodiversity and phylogenetic
relationships of Common Krait (Bungarus caeruleus)
from Pakistan showing inter- and intra-specific variations
among different geographical regions of the world. More
diverse sampling and a larger number of samples with
more genomic data could help to further resolve the
taxonomic status of the Bungarus species in Pakistan.
This study also provides guidance for the correct
identification of these snakes with authentication using
molecular biology tools which will be helpful in the
development of effective and region-specific antivenoms
for such venomous snakes.
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Muhammad Rizwan Ashraf is a scholar at the University of Veterinary and Animal Sciences,
Lahore, Pakistan. Muhammad has an M.Sc. in Biochemistry and Ph.D. in Molecular Biology and
Biotechnology. His research interest is reptilian (especially snake) molecular phylogeny and genetic
biodiversity. Muhammad visited University of Texas at Arlington, Texas, USA as a research scholar
under the International Research Support Initiative Program, funded by the Government of Pakistan,
and his Ph.D. work involved four of the most venomous snakes of Pakistan: Black Cobra, Common
Krait, Saw-scaled Viper, and Russell’s Viper. He is seeking further challenges to expand his skills
within a progressive and fast-growing environment that uses state-of-art technologies while enhancing
his proven abilities and dedication to team motivation.
Asif Nadeem is an Associate Professor at the University of Veterinary and Animal Sciences, Lahore,
Pakistan. Asif had the privilege of receiving research training from the University of Wisconsin—
Madison, Wisconsin, USA, and he has maintained a vigorous research program in the genetics of
animals of agricultural importance. His research has generated many publications in peer-reviewed
journals, and he has presented his research work at various national and international forums. Dr.
Nadeem’s efforts were recognized by his receipt of the Research Productivity Award from the Pakistan
Commission of Science and Technology. He is an internationally known researcher in the field of
animal genetics and genomics, and has served as an editor and reviewer for many different scientific
December 2019 | Volume 13 | Number 2 | e205
Amphib. Reptile Conserv.
Ashraf et al.
Eric Nelson Smith is a Professor at University of Texas at Arlington, Texas, USA. Eric’s current
research interest focuses on the Exploration and Speciation in the Volcanoes of the Indonesian Ring
of Fire: a Large-Scale Inventory of the Herpetofauna of the Highlands of Sumatra and Java. As a
benefit to the scientific community, this project is producing modern specimen repositories in the two
participating countries and web-based resources for identification and conservation, as well as for
genetic and biodiversity work. Many of these efforts have been directed toward the systematics and
taxonomy of venomous snakes. Eric has participated in the Threatened Amphibians of the World project
(https://portals.iucn.org/library/node/9186) and the International Union for the Conservation of Nature
(IUCN) Red List Assessment of Reptile Species, particularly with species of Asian coral snakes.
Maryam Javed is an Assistant Professor at the University of Veterinary and Animal Sciences, Lahore,
Pakistan. She has received many academic and scientific awards, including a gold medal in D.V.M.., Star
Laureate Award, Nestle Award, Tufail Muhammad Award, Best Student in Academics Award from the
Chancellor, Governor of Punjab, and the all Pakistan Quid Talent Award. Maryam’s current research
interest focuses on the identification of genes of economic importance in dairy animals.
Utpal Smart hails from Pondicherry, a sleepy coastal town (of Life of Pi fame) in southern India. Utpal’s
formal training in biology began with an M.Sc. in Ecology from Pondicherry University, India, in 2008,
followed by a Ph.D. in Quantitative Biology from the University of Texas at Arlington, USA, in 2016. His
doctoral training primarily involved using computational methods to investigate questions in molecular
ecology using a combination of macro- and micro-evolutionary approaches. As a postdoctoral research
associate at University of North Texas Center for Human Identification (UNTCHI), Utpal is helping to
create the Mitochondrial Mixture Database and Interpretation Tool (MMDIT)—a bioinformatic pipeline
for deconvoluting mitochondrial DNA mixtures and using computational phylogenetic and population
genetic methods on human microbiome data to leverage them as forensic tools.
Tahir Yaqub is a Senior Member of the University of Veterinary and Animal Sciences (UVAS), Lahore,
Pakistan, and has over 25 years of scientific experience in controlling infectious diseases of livestock,
including those caused by influenza viruses. Tahir did a postdoc at the Institute of Public Health, United
Kingdom, and his research interests include investigating the biological health risks of various agents in
public and animal health. His laboratory has postgraduate students with expertise in molecular biology
and serves as a hub for training. Currently, Tahir is investigating the prevalence and control of various
diseases of public health importance.
Abu Saeed Hashmi, Ph.D., is a well-known academician, researcher, and mentor in the field of
Biochemistry. Abu’s major area of research is in the bioconversion of agricultural/industrial waste to
value added products. Abu has supervised many postgraduate students and has contributed significantly
to this field. His work on bioconversion, Alfa toxins, bio-wastes, and production of biomass has been
published and widely cited in many prominent research journals.
Panupong Thammachoti graduated from the University of Texas at Arlington, USA, in the Quantitative
Biology Program (Ecology and Systematics). Panupong’s work used multiple approaches including
morphology, molecular phylogeny, and ecology, for solving taxonomic problems. As a lecturer at
Chulalongkorn University, Thailand, he is interested in several research topics focusing on the diversity
of amphibians and reptiles. Panupong has several scientific recognitions, such as a scholarship from the
Human Resource Development in Science Project (Science Achievement Scholarship of Thailand, SAST);
International Training Course-New Trends and Methodology in Animal Ecology and Conservation
Biology; International Society of Zoological Sciences, Beijing, China; The Professor Dr. Tab Nilanidhi
Foundation Award for outstanding academics, Faculty of Science, Chulalongkorn University; and the
best oral presentation award, JSPS CORE-TO-CORE PROGRAM at the 5th International Symposium
on Asian Vertebrate Species Diversity, Thailand.
211 December 2019 | Volume 13 | Number 2 | e205
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 212-216 (e206).
Daboia russelii (Reptilia: Squamata) in remote parts of Gujjar
Village Miandam, Swat, Khyber Pakhtunkhwa, Pakistan
12,*Wali Khan and 2Bashir Ahmad
'Department of Zoology, University of Malakand lower Dir, Khyber Pakhtunkhwa, PAKISTAN *Department of Zoology, Hazara University,
Mansehra, PAKISTAN
Abstract.—Snakes are widely perceived with fear by the general public in Pakistan, and they are often killed
on sight. The present study examines the range extension of Daboia russelii in remote parts of Gujjar village
Miandam Swat, Pakistan. Seven snakes were collected, including three which were attacked and injured by
the local men, and four others observed in the natural habitats in four localities: Karoo, Kalandori, Chharr, and
Dhop, from June to September in both 2016 and 2017. Morphometric analysis, details of the coloration, and
photographs of the snakes are provided. Russell’s Vipers were seen frequently in grasslands, cultivated fields,
and areas near human residences. These snakes were mostly seen after sunset. This species has also been
reported from other parts of Pakistan, but the present records represent a new locality.
Keywords. Russell’s Viper, Viperidae, morphometric analysis, range extension, snake, venomous
2 2 2
Citation: Khan W, Ahmad B. 2019. Daboia russelii (Reptilia: Squamata) in remote parts of Gujjar Village Miandam, Swat, Khyber Pakhtunkhwa,
Pakistan. Amphibian & Reptile Conservation 13(2) [General Section]: 212-216 (e206).
Copyright: © 2019 Khan and Ahmad. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 3 August 2018; Accepted: 25 March 2019; Published: 6 December 2019
Snakes are the most reviled of vertebrates, widely
perceived by the public as dangerous and harmful. The
2,700 species of snakes known to science include 375—
400 venomous species, of which approximately 200
species are considered life-threatening to man and other
animals. Snakes of the families Elapidae, Crotalidae,
and Viperidae are venomous (Durand 2004; Vidal et al.
2009).
Russell’s Viper is named as Daboia russelii in honor
of Patrick Russell (1726-1825). Daboia russelii is an
infamous venomous snake of the Old World, found in
Bangladesh, Cambodia, China, Indonesia, Myanmar,
Nepal, Pakistan, Sri Lanka, Taiwan, and Thailand
(McDiarmid et al. 1999). In Pakistan it occurs from the
Indus Valley to the Kashmir, and east to Bengal. This
snake is frequently found in Thatta District, Sindh, and
at low elevations in Punjab, but no published report is yet
available from the northwestern parts of Pakistan.
Relatively few studies have been conducted on the
fauna of Swat, and even fewer studies are associated
with the reptilian fauna of the region (Smith 1943;
Minton 1962, 1965; Mertens 1969, 1970; Khan 1982,
1984, 1985). More than fifty species of terrestrial snakes
are known from Pakistan (Khan 1980, 1982, 1997).
Khan (2002) conducted an extensive survey of different
climatic zones in Pakistan for herpetofaunal diversity.
Correspondence. * walikhan.pk@gmail.com
Amphib. Reptile Conserv.
The present study reports the existence of Russell’s
Vipers in the hilly areas of Swat Valley, Pakistan.
Village council Miandam is located at 35°03'12"N,
72°33'39"E, about 57 km from Saidu Sharif, District Swat,
Khyber Pakhtunkhwa, at an elevation of approximately
1,918 m asl. The study area (Fig. 1) falls under moist
temperate forest, thus receiving summer monsoon and
winter snow fall. Because of its cool climate and green
hillsides, the area is frequented by tourists (Forest
Working Plan 2013).
In village council Miandam, there are two sub-villages,
namely Gujjar village and Swati village. Four sites of the
Gujjar village were surveyed from June to September in
2016 and 2017 (Fig. 2). The snake specimens (Table 1)
were either collected dead following their attack by the
local people, or recorded with visual observations using
the method of Campbell and Christman (1982).
The photographs of specimens shown here (Fig.
3) were taken using a Nikon Coolpex L330 camera.
Morphometric analysis of the snake specimens collected
dead were recorded using a digital caliper (Precision
145). The specimens observed were identified with the
help of keys provided by Khan (2002). The general
characteristics of Daboia russelii specimens from the
four localities of Gujjar village Miandam, Swat (2016-
2017) are as follows:
December 2019 | Volume 13 | Number 2 | e206
Khan and Ahmad
Fig. 1. Map of Khyber Pakhtunkhwa, red circle shows the study area in the District Swat within the province.
Table 1. Records of the seven specimens observed by month and village.
2016 2017
Dhop Chharr Karoo Kalandori Dhop Chharr Karoo Kalandori
January
February
March
April
May
June live
July dead
August dead live live dead
September live
October
November
December
Amphib. Reptile Conserv. 213 December 2019 | Volume 13 | Number 2 | e206
Fig. 2. Colle
Daboia russelii in northwestern Pakistan
%,
a
a Re
ction sites
Head: Longer rather than broad, distinctly wider
than neck.
Body: Stout, flattened dorsoventrally, tapering
evenly both posteriorly and anteriorly.
Snout: Bluntly pointed, snout-vent length 1,022—
1,075 mm, tail 215-223 mm.
Rostral: About twice as high as wide.
Nostril: Large, crescent shaped in large nasal
scale.
Supraocular scale: Entire, not divided.
Supralabials: 12, separated from eye by three or
four rows of small scales.
Infralabials: 14.
Anterior chin shield: Short and wide, posterior
not well differentiated from surrounding scales.
Dorsal scales: Keeled except for lowest row, 29—
31 rows at mid-body, reduction posteriorly to 23
or 21 rows, usually an anterior reduction of two
or four rows.
Ventrals: 165-173.
Total body length: 76.2 cm, tail length 15.2 cm
(16% of total body length).
Coloration:
¢ Dorsal ground color light tan to sandy.
¢ Chest net spots with black or dark brown
Amphib. Reptile Conserv.
of Daboia russelii in Guar village Miandam, Swat, KP, Pakistan. (A) Karoo, 35°3'32"N 72°33'11"E: (B)
Kaalandori, 35°3'31"N 72°32'21"E; (C) Chhar 35°3'34"N 72°33'12"E; (D) Doop, 35°3'23"N 72°32'58"E.
borders and edge creamy, these spots fused
to a greater or lesser extent, lateral series of
similar but smaller spots below which are
scattered dark flecks with light edges.
¢ Two large dark spots at base of head.
¢ A light V-shaped mark with its apex on top
of snout.
¢ Labial sides of snout mottled with brown and
cream.
¢ Belly whitish with black semilunar spots.
¢ Chin or throat white.
¢ Many scales topped with black.
The fauna and flora of Pakistan is Oriental, Palearctic,
Ethiopian, and Central Asian in nature, with many
endemic forms (Smith 1931; Khan 1980). In Pakistan
the complex of habitats is diverse, including oceans,
swamps, rivers, lakes, flood plains, arid plains, sand and
rocky deserts; tropical thorn, tropical dry deciduous,
subtropical dry, subtropical arid, subtropical pine, dry and
moist temperate subalpine forests; grassy tundra and cold
deserts. Moreover, most of the habitats are now heavily
influenced by anthropogenic activities which negatively
affect the fauna and flora of the country (Baig 1975).
The present study describes seven specimens of
214 December 2019 | Volume 13 | Number 2 | e206
Khan and Ahmad
Russell’s Vipers from four localities in the study area,
including two specimens each from Dhoop, Chhar, and
Karoo, and one specimen from Kalandori Gujjar Village
Miandam, Swat, Pakistan. Russell’s Viper is one of the
most widespread of Asiatic venomous snakes. While
surveying the literature no published records for this
species are available in Swat Valley, Pakistan. Therefore,
the present study documents the presence of this species
in the hilly areas of Swat Valley.
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Science Research Desert, Punjab, Pakistan. Journal of
the Bombay Natural History Society 82: 144-148.
Campbell HW, Christman SP. 1982. Field techniques for
herpetofaunal community analysis. Wildlife Research
Amphib. Reptile Conserv.
oat
Fig. 3. Photos of the dead Daboia russelii specimens from Gujjar village Miandam, Swat, KP, Pakistan. (A, B) Dorsal views, (C,
D) Fangs, (E) Black spots on ventral side, (F) Anal orifice with tail showing a zip-like structure.
Report 13: 193-200.
Durand JF. 2004. The origin of snakes. Pp. 187
In: Geoscience Africa 2004. University of the
Witwatersrand, Johannesburg, South Africa.
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Project, Village Plan, Miandam, Pakistan. pp. 7-13.
Khan MS. 1980. Affinities and zoogeography of herptiles
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reptiles of Pakistan. Part III: Serpentes (Ophidia).
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and Reptiles from Cholistan Division. Bulletin
Number 5. Botany Department, Pakistan Forest
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Daboia russelii in northwestern Pakistan
Institute, Peshawar, Pakistan.
Khan MS. 1997. A new toad of genus Bufo from the foot
of Siachin Glacier, Baltistan, northeastern Pakistan.
Pakistan Journal of Zoology 29: 43-48.
Khan MS. 2002. A Guide to the Snakes of Pakistan.
Edition Chimaira, Frankfurt am Main, Germany. 265
p.
Mertens R. 1969. Die Amphibien und Reptilien West-
Pakistans. Stuttgarter Beitrdge zur Naturkunde 197:
1-96.
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Pakistans. Stuttgarter Beitrdge zur Naturkunde 216:
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Minton SA, Anderson S. 1965. A new dwarf gecko
(Tropiocolotes) from Balochistan. Herpetological
Bulletin 21: 59-61.
Minton SA. 1962. An annotated key to the amphibians
and reptiles of Sind and Las Bela, West Pakistan.
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Smith MA. 1931. The Fauna of British India, including
Ceylon and Burma. Reptilia and Amphibia. Volume I.
Taylor and Francis, London, United Kingdom. 85 p.
Smith MA. 1943. The Fauna of British India, Ceylon and
Burma. Reptilia and Amphibia. Volume III. Taylor
and Francis, London, United Kingdom. 583 p.
Vidal N, Rage JC, Couloux A, Hedges SB. 2009. Snakes
(serpents). The Time Tree of Life 23: 390-397.
Wali Khan currently works as Assistant Professor in the Department of Zoology, University
of Malakand, Lower Dir, Khyber Pakhtunkhwa, Pakistan. Wali is interested in understanding
the helminth parasite fauna as a factor threatening the conservation of amphibian and reptile
Bashir Ahmad is currently a research scholar in the Department of Zoology, University of Hazara,
Mansehra, Pakistan, in collaboration with the Laboratory of Parasitology, Department of Zoology,
University of Malakand, Lower Dir, Khyber Pakhtunkhwa, Pakistan. Bashir is interested in
understanding the host-parasite relationships of vertebrates as a factor threatening conservation.
December 2019 | Volume 13 | Number 2 | e206
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 217-226 (e207).
of
Ry
ptile-con*
Native anuran species as prey of invasive American Bullfrog,
Lithobates catesbeianus, in Brazil: a review with new
predation records
12,*Fabricio H. Oda, *Vinicius Guerra, “Eduardo Grou, *Lucas D. de Lima,
5SHelen C. Proenga, °Priscilla G. Gambale, **Ricardo M. Takemoto, ‘Caué P. Teixeira,
‘Karla M. Campiao, and *Jean Carlo G. Ortega
'Departamento de Quimica Biolégica, Programa de Pés-graduacgdo em Bioprospec¢do Molecular, Universidade Regional do Cariri, Campus
Pimenta, 63105-000, Crato, Ceard, BRAZIL *Departamento de Quimica Bioldgica, Laboratorio de Zoologia, Universidade Regional do Cariri,
Campus Pimenta, Crato, Ceard, BRAZIL *Departamento de Ecologia, Laboratorio de Herpetologia e Comportamento Animal, Instituto de
Ciéncias Biologicas, Universidade Federal de Goids, Campus Samambaia, Goidnia, Goids, BRAZIL *Centro de Ciéncias Bioldgicas, Nucleo de
Pesquisas em Limnologia, Ictiologia e Aquicultura, Laboratorio de Ictioparasitologia, Universidade Estadual de Maringa, Maringa, Parana,
BRAZIL *Centro de Ciéncias Biologicas, Programa de Poés-graduacdo em Biologia Comparada, Universidade Estadual de Maringd, Parana,
BRAZIL ‘Universidade Estadual de Mato Grosso do Sul, Dourados, Mato Grosso do Sul, BRAZIL ‘Departamento de Zoologia, Laboratorio
de Ecologia de Interagées Antagonistas, Universidade Federal do Parana, Centro Politécnico, Curitiba, Paranda, BRAZIL *Departamento de
Ecologia, Programa de Pos-graduacgdo em Ecologia e Evolugdo, Instituto de Ciéncias Bioldgicas, Universidade Federal de Goids, Campus
Samambaia, Goidnia, Goids, BRAZIL
Abstract.—The American Bullfrog (Lithobates catesbeianus) is widely distributed throughout the world as an
invasive species, and causes negative impacts on the fauna resulting from its voracious predatory activity.
This study documents two new predation reports and reviews the previous predation reports of the American
Bullfrog on native Brazilian anurans. Twenty-one species of native anurans were recorded as American Bullfrog
prey in Brazil. A positive correlation was found between the number of native anurans preyed on by American
Bullfrog and the respective family or number of species per genus. Most of the prey species are small or
medium-sized, and the results suggest that the generalist diet and intraguild predation may have favored the
widespread establishment of the American Bullfrog.
Keywords. Amphibia, Atlantic Forest, biological invasion, conservation, global change, intraguild predation, exotic
species
Citation: Oda FH, Guerra V, Grou E, de Lima LD, Proenga HC, Gambale PG, Takemoto RM, Teixeira CP, Campiao KM, Ortega JCG. 2019. Native
anuran species as prey of invasive American Bullfrog, Lithobates catesbeianus, in Brazil: a review with new predation records. Amphibian & Reptile
Conservation 13(2) [General Section]: 217-226 (e207).
Copyright: © 2019 Oda et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0
International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any me-
dium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as
follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 8 February 2017; Accepted: 23 June 2019; Published: 20 December 2019
Introduction
Biological invasions represent a major threat to natural
ecosystems and their respective biodiversity, human
health, and food security (UCN 2012). In this context,
the American Bullfrog, Lithobates catesbeianus (Shaw,
1802), is a globally widespread introduced species (Lowe
et al. 2004). It is native in North America, occurring
from eastern Canada and the central and eastern United
States to northeastern Mexico (Quiroga et al. 2015).
The introduction of L. catesbeianus in non-native
environments has direct (e.g., predation and competition)
and indirect (e.g., parasites, disease introduction, and
biotic homogenization) impacts on biodiversity (Batista
2002; Batista et al. 2015; Kiesecker and Blaustein 1998;
Kraus 2009).
Lithobates catesbeianus 1s a voracious predator whose
diet includes a wide variety of prey (Boelter and Cechin
2007; Boelter et al. 2012; Silva et al. 2009). Juveniles
feed mainly on insects (Silva et al. 2009), whereas adults
prey upon invertebrates and small vertebrates, such as
fish, reptiles, birds, and mammals (Quiroga et al. 2015).
Correspondence. ‘fabricio_oda@hotmail.com (FHO), vinicius.guerrabatista@gmail.com (VG), eduardogrou@hotmail.com (EG), lucasdu-
artelima@hotmail.com (LDL), helencassia23@hotmail.com (HCP), priscillagambale@gmail.com (PGG), takemotorm@nupelia.uem. br (RMT),
caue.cpt@gmail.com (CPT), karla_mcamp@yahoo.com. br (KMC), ortegajean@gmail.com (JCGO)
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e207
Impact of bullfrogs on native anurans in Brazil
American Bullfrogs are considered opportunistic feeders,
also preying on amphibians, including conspecifics and
other species (Silva et al. 2011; Toledo et al. 2007).
The American Bullfrog is now established in
nearly 40 countries around the world (Frost 2019;
Kraus 2009). In Brazil, the first specimens were
introduced in 1935 for commercial exploitation at
the municipality of Itaguai, Rio de Janeiro state
(Vizotto 1984). The introduction of the American
Bullfrog for commercial frog farming was due to its
fast reproduction and greater development in captivity
compared to native species. It occurs mainly in the
southern and southeastern Brazilian states because of
its easy adaptation to the climatic conditions (Vizotto
1984). Approximately 2,000 commercial frog farms
were active in the early 1990s in Brazil, but many
closed their activities because of low profitability
(Lima and Agostinho 1988), which led to American
Bullfrog specimens being abandoned or released into
the natural environments, and consequently several
accidental invasions have occured in Brazil (Both et
al. 2011).
Populations of Lithobates catesbeianus are now
known to be present in 155 Brazilian municipalities
(Both et al. 2011; Instituto Horus 2016), a context in
which many studies have revealed the localized impacts
of its predatory activity on native anuran fauna (Batista
et al. 2015; Boelter and Cechin 2007; Boelter et al.
2012; Leivas et al. 2012; Silva et al. 2011). In addition,
global-scale studies have demonstrated trophic niche-
width shifts in bullfrog populations from both native and
invaded areas (Bissattini and Vignoli 2017), as well as the
effects of the interactions between bullfrogs and crayfish
on native amphibians (Bissattini et al. 2018, 2019; Liu
et al. 2018). However, studies summarizing data on the
predation of native anurans by American Bullfrogs have
yet to be presented; therefore, knowledge on the impact
and the native anuran species preyed upon by such an
invasive frog may benefit our understanding of their
predator-prey relationships.
Herein, the predation of Boana raniceps and
Phyllomedusa_ distincta by males of Lithobates
catesbeianus are reported, and the available literature
on the predation of native anurans by the invasive frog
L. catesbeianus in Brazil is reviewed. An overview on
the number and identities of native species reported as
prey and the potential impact of the American Bullfrog
on native anurans are provided.
Material and Methods
Bibliographic Review
An extensive literature review was conducted to find
scientific articles, natural history notes, and theses which
contain reports on the predation of native anurans by the
Amphib. Reptile Conserv.
invasive American Bullfrog Lithobates catesbeianus in
Brazil. The sources included articles or natural history
notes published in Herpetological Review (1967-2018),
Herpetological Bulletin (2008-2018), Herpetology
Notes (2008-2018), and South American Journal of
Herpetology (2006-2018). Searches were also conducted
in Web of Science using the following query: (“Rana
catesbeiana”’ OR “Lithobates catesbeianus”) AND
(“diet” OR “feeding biology” OR “predation”, applied in
the field “topic” on 30 December 2018, without applying
any filters for year or other parameters. Considering
that predation attempts would not necessarily result in a
predation event (Toledo et al. 2007), reports of predation
attempts in the field, laboratory experiments, or captivity
were not included. Masters and doctoral papers in digital
format were obtained from the library databases of
Brazilian universities (especially Universidade Estadual
Paulista and Universidade Regional de Blumenau) by
using the search terms mentioned above in the Google
search engine.
The Web of Science query resulted in 159 studies,
three of which met the criteria and were included in the
study. Eight additional predation records were selected for
inclusion in the study by searching the selected journals
(six studies) and the library databases of Brazilian
universities (two studies). Information was extracted
from each diet analysis (1.e., the diet was described
through the analyses of stomach contents or predation
records), study location, anuran prey species, geographic
range, and body size. The geographic range follows the
list of anuran species for each Brazilian federal state
and the biomes proposed in Toledo and Batista (2012).
The body sizes of anuran species follow the size values
available in Uetanabaro et al. (2008) and Haddad et
al. (2013). The spatial distribution map of Lithobates
catesbeianus invasive populations and predation reports
were generated with 155 occurrence points for American
Bullfrog in Brazil, obtained from Both et al. (2011) and
Instituto Horus (2016).
Data Analysis
The relation between the number of native anuran
Species preyed upon by the American Bullfrog and the
number of native anurans per family or genus was tested
with a Pearson correlation analysis. The numbers of
native anuran prey species per family and genus were
compiled following the Frost (2019) database. Toledo et
al. (2007) stated that a positive correlation between the
number of predation events and taxonomic richness may
be a proxy for search representativeness, by reasoning
that taxa with more species would be more frequently
predated by chance (1.e., a sampling effect). Such a
correlation could indicate the possible mechanisms of L.
catesbeianus impacts on native biota apart from search
representativeness.
December 2019 | Volume 13 | Number 2 | e207
Oda et al.
: : j
4 a Z -— |
Fig. 1. Adult Lithobates catesbeianus swallowing an adult
Boana raniceps in an artificial permanent pond within pasture
area in southern Brazil.
Results
Field Observations and New Predation Records
An adult Lithobates catesbeianus swallowing an adult
Boana raniceps (Fig. 1) was recorded on 11 October
2014 at 2100 h, in an artificial permanent pond inside a
pasture area (23°20’38”S, 51°52’07”W), in the northern
region of Parana state, southern Brazil. Although the
specimens escaped, voucher specimens of the native
anuran species and L. catesbeianus had been previously
collected by Affonso et al. (2014) and stored at the
Amphibian Collection from the Zoology and Botany
Department, Bioscience Institute, Universidade Estadual
Paulista, Rio Claro, Sao Paulo, Brazil.
A second predation event recorded a male adult
specimen of Bullfrog swallowing a treefrog (Fig. 2A).
The specimen was collected during an L. catesbeianus
survey on 22 January 2019, at 2200 h, in an artificial
permanent pond in a rural property at Iporanga, southern
Sao Paulo state, southeastern Brazil (24°35’01.2”S,
48°36’00.4”W). The L. catesbeianus specimen was taken
to the laboratory where the anuran prey was removed and
identified as an adult Phyllomedusa distincta (Fig. 2B).
removed from the oral cavity of L. catesbeianus.
Amphib. Reptile Conserv.
Exploratory Analysis
Overall, 11 publications reported predation events,
corresponding to 41 records of native anurans as prey
of L. catesbeianus (Table 1). Nine of the publications
discussed the diet in a broader sense, and two were
natural history notes reporting predation events. Most
of the records occurred in Minas Gerais state (39%),
followed by Rio Grande do Sul (~32%), Parana (~12%),
Sao Paulo (~12%), and Santa Catarina (~5%), at sites
inside the Atlantic Forest, in addition to another site in
a transition zone between Cerrado and Atlantic Forest
(Fig. 3, Table 1).
This survey accounted for 21 anuran species as prey
of L. catesbeianus, all widely distributed and possibly
coexisting with American Bullfrogs in their breeding
sites. The anuran family Hylidae had the highest number
of species (11 species), followed by Leptodactylidae (four
species), Bufonidae and Microhylidae with two species
each, and Odontophrynidae and Phyllomedusidae with
one species each. Lithobates catesbeianus often preyed
on medium-sized species, but small-sized species were
also preyed upon (Table 1).
A positive correlation was found between the number
of native anuran species preyed on by American Bullfrog
and genus richness (r = 0.71, P = 0.01), whereas at the
family level no relationship was found (r = 0.53, P =
0.22). Thus, considering the studies analyzed, genera
with higher numbers of species presented more potential
prey for American Bullfrogs in Brazil.
Discussion
Most of the predation records found in this review came
from a few studies which assessed the overall dietary
composition of L. catesbeianus, and revealed that the
diet of these invasive frog populations is represented
by a wide variety of native anuran species (Boelter and
Cechin 2007; Silva et al. 2009, 2010, 2011). Only two
predation records of L. catesbeianus and native anurans
in the field were found, probably due to some difficulty
cal
Fig. 2. (A) Predation of an adult Phyllomedusa distincta by Lithobates catesbeianus, (B) Adult P. distincta partially digested,
December 2019 | Volume 13 | Number 2 | e207
Impact of bullfrogs on native anurans in Brazil
0°
10° S$
20°S
Biomes
[ Amazon
[ Caatinga
[| Cerrado
Atlantic Forest
| Pampa
[| Pantanal
Ee
30° S
70° W 60° W
50° W 40° W
Fig. 3. Spatial distribution of Lithobates catesbeianus invasive populations and predation reports of native anurans in Brazil. White
circles: American Bullfrog populations in Brazil (Both et al. 2011; Instituto Horus 2016); yellow stars: predation reports of adult
Boana raniceps and adult Phyllomedusa distincta in southern and southeastern Brazil; light green circles: locations of 41 published
predation records.
in recording and quantifying these events in the field
(Pombal Jr. 2007).
The predicted potential occurrence of L. catesbeianus
in Brazil represents its current distribution in the southern
and southeastern regions in the Atlantic Forest, with
potential areas for colonization remaining in the central
and northeastern regions (Giovanelli et al. 2008; Both et
al. 2011). The results showed that all predation records
occurred at sites in southern and southeastern Brazil,
regions with higher numbers of research centers, thus
contributing a disproportionately greater number of field
studies.
Native anurans recorded as prey of American
Bullfrogs share the same breeding sites. Silva et al.
(2011) had found a spatial overlap in microhabitat use
between native species and American Bullfrogs during
the reproductive season. American Bullfrogs may also
overlap with native amphibians in diet composition
Amphib. Reptile Conserv.
(Bissattini et al. 2019). This may lead to a potential
competition, and may have a direct influence on
community composition patterns since the intrinsic
ecological properties of organisms determine the niche
overlap between species in the communities (Vignoli
and Luiselli 2012; Vignoli et al. 2017). Additionally, the
predation on other anuran species by L. catesbeianus can
represent an example of intraguild predation (Polis et al.
1989), a process that may facilitate the establishment of
the American Bullfrog (Bissattini et al. 2018), as found
in other disparate introduced taxa, such as ladybird
beetles (Snyder et al. 2004) and fish (Pereira et al. 2015).
Intraguild predation can benefit the establishment of L.
catesbeianus by reducing the competitive pressure by
direct predation of the other anuran species.
The number of prey species had a positive correlation
with the number of species per genus, in which the
family Hylidae had the highest number of species as
December 2019 | Volume 13 | Number 2 | e207
Oda et al.
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Impact of bullfrogs on native anurans in Brazil
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December 2019 | Volume 13 | Number 2 | e207
222
Amphib. Reptile Conserv.
Oda et al.
prey of L. catesbeianus. Boelter et al. (2012) found
that 60% of the prey records corresponded to Hylidae
Species, suggesting that this group suffers higher
predation pressure. At least two non-mutually exclusive
hypotheses may explain these patterns by relating family
(i.e., richness, abundance) and species traits (1.e., body
size) to L. catesbeianus predation rates, involving
species traits that are often phylogenetically correlated
(Martins and Hansen 1997). Firstly, it is possible that
Hylidae species are often preyed upon due to their higher
species richness in comparison to other families, which
is a plausible hypothesis if we assume that predation
rates can be proportional to prey abundance or richness
(i.e., higher predation rates in higher resource availability
conditions; Jacobsen et al. 2014; Madahi et al. 2015).
Secondly, Hylidae species may have a higher predation
rate because of their smaller size relative to species from
other families (e.g., Bufonidae). Predators that feed
on whole animals, such as the American Bullfrog, are
limited by the prey’s body size. Experimental evidence
indicates that larger specimens of L. catesbeianus feed
preferentially on smaller, rather than on large-sized,
native anurans (Wang et al. 2007), suggesting a size-
based selection of prey species. Partially related to this
hypothesis, our results suggest a higher amount of small
and medium-sized species as American Bullfrog prey.
Therefore, the preference for prey of a certain body size
may be proportionally related to the body size of the
predators, as observed in previous studies (Quiroga et al.
2015; Silva et al. 2011, 2009; Wang et al. 2007).
This survey found that all anuran species preyed upon
by L. catesbeianus have large geographic distributions,
occurring in various Brazilian states and biomes (Frost
2019; Toledo and Batista 2012). Both et al. (2014)
found that American Bullfrog abundance had a positive
relationship with communities that consisted of generalist
species (e.g., Physalaemus cuvieri, Dendropsophus
minutus), that were anthropogenically adapted and
broadly distributed in South America. Native anurans
with large geographic ranges (e.g., Rhinella diptycha,
Dendropsophus minutus, Boana faber, B. raniceps,
Scinax fuscovarius, and Physalaemus cuvieri) have also
been found in sympatry with Lithobates catesbeianus
elsewhere (Affonso et al. 2014).
Conclusions
This study indicated L. catesbeianus preys on at least
21 native anuran species in Brazil. Predation is one of
the major negative effects of Invasive species on native
communities. The quality of being a generalist feeder,
preying on many anuran species, has benefited the
successful colonization, establishment, and permanence
of the American Bullfrog in Brazil (and even worldwide;
e.g., Li et al. 2011; Monello et al. 2006; Quiroga et al.
2015). Native species of the family Hylidae may be more
susceptible to American Bullfrog predation because of
Amphib. Reptile Conserv.
their higher abundance and richness, and/or due to a
higher representation of small- to medium-sized species
relative to other anuran families. Knowledge on the
species most vulnerable to predation by the American
Bullfrog can enable better prediction of the negative
impacts of such an invasive species on native anuran
communities.
Acknowledgements.—The authors would like to thank
Centro Universitario de Maringa for having granted us
access to the Fazenda Escola UniCesumar, and Bruno
Barreto for assisting with Fig. 3. Fabricio H. Oda received
a postdoctoral fellowship from Funda¢ao Cearense de
Apoio ao Desenvolvimento Cientifico e Tecnoldgico/
Coordenacéo de Aperfeicoamento Pessoal de Nivel
Superior — CAPES (Grant number 88887.162751/2018-
00). Vinicius Guerra received fellowships from CAPES,
and Helen C. Proenca and Jean Carlo G. Ortega received
fellowships from Conselho Nacional de Desenvolvimento
Cientifico e Tecnologico — CNPq. Ricardo M. Takemoto
received a CNPq grant of research productivity
fellowship as well. Finally, the authors would like to
thank the Instituto Chico Mendes de Conservacao da
Biodiversidade/Sistema de Autorizacéo e Informacao
em Biodiversidade for providing us with the collecting
permit (process #23866-1).
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2006. Growth and behavioral responses of tadpoles
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Nori J, Urbina-Cardona JN, Loyola RD, Lescano JN,
Leynaud GC. 2011. Climate change and American
Bullfrog invasion: What could we expect in South
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746(1): 223-231.
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and evolution of intraguild predation: potential
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Pombal Jr JP. 2007. Notas sobre predagcéo em uma
taxocenose de anfibios anuros no sudeste do Brasil.
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Quiroga L, Moreno MD, Cataldo AA, Aragon-Traverso
JH, Pantano MV, Olivares JPS, Sanabria EA. 2015.
Diet composition of an invasive population of
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1,703—1,716.
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Silva ET, Both C, Filho OPR. 2016. Food habits of
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in sympatry in southeastern Brazil. South American
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Brazil: spatial variation and effect of microhabitat use
by prey. South American Journal of Herpetology 6(1):
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Silva ET, Reis EP, Feio RE, Filho OPR. 2009. Diet of
the invasive frog Lithobates catesbeianus (Shaw,
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Brazil. South American Journal of Herpetology 4(3):
286-294.
Silva ET, Reis EP, Santos PS, Feio RN. 2010.
Lithobates catesbeianus (American Bullfrog). Diet.
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Snyder WE, Clevenger GM, Eigenbrode SD. 2004.
Intraguild predation and successful invasion by
introduced ladybird beetles. Oecologia 140(4): 559-
565.
Toledo LF, Batista RF. 2012. Integrative study of
Brazilian anurans: geographic distribution, size,
environment, taxonomy, and conservation. Biotropica
44(6): 785-792.
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prey: an exploratory analysis and size relationships
between predators and their prey. Journal of Zoology
271(2): 170-177.
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Campos Z. 2008. Guia de Campo dos Anuros do
Pantanal Sul e Planaltos de Entorno. Editora UFMS/
UFMT, Campo Grande, MS, Brazil. 196 p.
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Fabricio Hiroiuki Oda is a postdoctoral research fellow in the Programa de Pos-graduacéo em
Bioprospec¢ao Molecular (URCA — Universidade Regional do Cariri, Brazil) and research collaborator
in the Laboratorio de Ictioparasitologia do Nucleo de Pesquisas em Limnologia, Ictiologia e Aquicultura
(UEM — Universidade Estadual de Maringa, Brazil). His primary areas of interest are the natural history,
ecology, and parasitology of fish, amphibians, and reptiles.
Vinicius Guerra is a postdoctoral researcher in the Laboratorio de Herpetologia e Comportamento Animal
(UFG — Universidade Federal de Goias, Brazil). His primary areas of interest are the study of community
ecology, animal behavior, natural history, and bioacoustics, with a particular focus on amphibians.
Eduardo Grou is a volunteer researcher in the Laboratorio de Ictioparasitologia do Nucleo de Pesquisas em
Limnologia, Ictiologia e Aquicultura (UEM — Universidade Estadual de Maringa, Brazil). His primary areas
of interest are the ecology and parasitology of chelonians.
December 2019 | Volume 13 | Number 2 | e207
Impact of bullfrogs on native anurans in Brazil
Lucas Duarte de Lima is a Master’s student fellow in the Programa de Pos-gradua¢ao em Biologia Comparada
(UEM — Universidade Estadual de Maringa, Brazil). His primary area of interest is amphibian diversity.
Helen Cassia Proenca is a Doctoral student fellow in the Programa de Pos-graduacao em Biologia Comparada
(UEM — Universidade Estadual de Maringa, Brazil). Her primary area of interest is snake diversity.
Priscilla Guedes Gambale is a researcher in the Departamento de Biologia (UEMS —Universidade Estadual
de Mato Grosso do Sul, Brazil). Her primary area of interest is the ecology of amphibians, with a particular
focus on bioacoustics.
Ricardo Massato Takemoto is a researcher in the Laboratorio de Ictioparasitologia do Nucleo de Pesquisas
em Limnologia, Ictiologia e Aquicultura (UEM — Universidade Estadual de Maringa, Brazil) and advisor in
the Programa de Pés-gradua¢4o em Ecologia de Ambientes Aquaticos Continentais and the Programa de Pos-
gradua¢ao em Biologia Comparada (UEM — Universidade Estadual de Maringa, Brazil). His primary area of
interest is the study of parasites of aquatic organisms, including fish and amphibians.
Caué Pinheiro Teixeira is Master’s researcher in the Laboratorio de Ecologia de Interagées Antagonistas
(UFPR — Universidade Federal do Parana, Brazil). His primary areas of interest are ecology, herpetology,
parasitology, and biological invasion.
Karla Magalhaes Campiao is a researcher and coordinator of the Laboratorio de Ecologia de Interagdes
Antagonistas (UFPR — Universidade Federal do Parana, Brazil), and she supervises graduate students in
Ecology and Zoology. Her primary areas of interest are amphibian parasites and disease ecology.
Jean Carlo Goncalves Ortega is a postdoctoral researcher in the Programa de Pos-graduacéo em Ecologia
e Evolugaéo (UFG — Universidade Federal de Goias, Brazil). His primary areas of interest are community
ecology and biological invasions.
Amphib. Reptile Conserv. 226 December 2019 | Volume 13 | Number 2 | e207
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 227-238 (e208).
Biology of snakes of the genus Tretanorhinus:
an integrative review
12.*Mlarco D. Barquero and ‘*Viviana Arguedas
'Asociacion para la Conservacion y el Estudio de la Biodiversidad (ACEBIO), San José, COSTA RICA *Sede del Caribe, Universidad de Costa
Rica, Montes de Oca, San José, 2060, COSTA RICA +Sede de Occidente, Universidad de Costa Rica, Montes de Oca, San José, 2060, COSTA RICA
Abstract.—Many aspects of the biology of various snake species remain unknown, and the extent of this lack
of information is not always clear. As new research usually depends upon previous findings, the gaps in our
knowledge and the accuracy of published information are of major importance. Therefore, an analysis of all
available information on snakes of the genus Tretanorhinus, from both the literature and museum specimens,
is presented here to illuminate existing knowledge gaps. The database compiled from 87 documents referring
to snakes of this genus and 755 specimens held in scientific collections revealed major gaps and contradictory
information for all four species of this genus. Data on morphology, ecology, and natural history are completely
absent for 7. mocquardi and T. taeniatus, whereas confusing distribution reports exist for T. nigroluteus. The
potential consequences of these problems were determined, and some suggestions for correcting them are
addressed. Specifically, we consider that focused efforts on the validation of current species and subspecies,
field and lab studies of ecology and behavior, and estimations of population dynamics, are necessary.
Keywords. Colubridae, Dipsadidae, ecology, literature review, morphology, museum specimens, natural history, Rep-
tilia, Serpentes, taxonomy
Citation: Barquero MD, Arguedas V. 2019. Biology of snakes of the genus Tretanorhinus: an integrative review. Amphibian & Reptile Conservation
13(2) [General Section]: 227-238 (e208).
Copyright: © 2019 Barquero and Arguedas. This is an open access article distributed under the terms of the Creative Commons Attribution License
[Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 24 June 2018; Accepted: 6 December 2018; Published: 10 December 2019
Introduction
Fieldwork with snakes usually poses several challenges
and more attention has focused on snake species from
temperate areas than those from the tropics (Avila et al.
2006), despite the latter having higher diversity (Greene
1997). This bias has resulted in a lack of key information
on essential aspects of the ecology, natural history, and
behavior of many species. The collection of such data
is a time-consuming and difficult task, as many snake
species have cryptic habits and occur in low densities
(Greene 1997). However, the lack of basic information
for many snake species is a major concern, because this
information is crucial for making general interspecific
comparisons, establishing proper phylogenetic
relationships, determining population trends and
dynamics, and recognizing differences in behavior.
Therefore, reviewing the current state of knowledge
for a given species is imperative to identify the areas
that require more attention and to guide research and
conservation efforts in the proper direction.
Snakes of the genus Tretanorhinus are nocturnal,
aquatic species that have intrigued biologists for more
than a century (Cope 1861; Dumeéril et al. 1854). Their
habits and secretive behavior make them difficult to
study, so their biology remains largely unknown (Savage
2002; Schwartz and Henderson 1991). Currently, four
species are recognized in the genus: 7’ mocquardi
(Bocourt 1891), 7. nigroluteus (Cope 1861), 7: taeniatus
(Boulenger 1903), and 7: variabilis (Duméril et al.
1854). Although a handful of studies have increased
our knowledge about these species (e.g., Barquero et al.
2005; Dunn 1939; Henderson and Hoevers 1979; Villa
1970), the genus remains poorly studied.
Here we summarize and integrate all available
published information, highlight the gaps in our
knowledge of the biology of Tretanorhinus species,
and make suggestions to direct future research in
order to fill in these gaps. To achieve this, searches
were conducted to find all published material referring
directly (1.e., studies focused specifically on one or more
Tretanorhinus species) or indirectly (1.e., studies focused
on many taxa that mentioned one or more 7retanorhinus
Species as part of the topic) to snakes of this genus and
a database of key information was compiled (Appendix
1). The information mentioned in each study was
used to determine missing data for each species. Each
publication was classified using the following categories:
Correspondence. !** marco.barquero_a@ucr.ac.cr, | viviarguedas@gmail.com
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e208
Biology of Tretanorhinus species
—o mocquardi
=H nigroluteus
—®- taeniatus
—i-variabilis
Number of individuals
3
Number of individuals
(=
T T T T T T T T T ® T
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Fig. 1. Number of specimens of the four species of Tretanorhinus
according to (A) decade and (B) month of collection.
natural history, morphology, taxonomy, systematics,
ecology, distribution, biogeography, and reproduction.
In addition, data were obtained for specimens held
in scientific collections (Appendix 2) from the
HerpNet2 data portal (http://www.herpnet.org), Global
Biodiversity Information Facility (http://www. gbif.org),
Data Research Warehouse Information Network (http://
darwin.naturalsciences.be), and by directly contacting
collection curators. When available, the following data
were extracted: taxonomic classification, type status,
sex and age classes, country and locality of the point
of capture, latitude and longitude of the collection site,
date of collection, and remarks about the individual
collected.
Literature Review and Scientific Collections
The search for publications referring to 7retanorhinus
produced a total of 87 documents, although only 16
focused directly on species of the genus (Appendix
1). Most of the documents focused on general aspects
of natural history (31%), taxonomy (21.8%), and
biogeography (20.7%), and the vast majority referred
to T. nigroluteus or T: variabilis, with only a handful of
studies mentioning 7. mocquardi (n = 12) or T: taeniatus
(n= 8).
A database with information for a total of 755
specimens of Tretanorhinus held in 31 scientific
collections was compiled (Appendix 2). Most records
corresponded to 7: nigroluteus (n = 350) or T: variabilis
(n= 357), and only a few were available for 7. mocquardi
(n= 25) or 7. taeniatus (n = 9). In addition, eight records
Amphib. Reptile Conserv.
were identified only to the genus level, and six were
mistakenly identified as Tretanorhinus agassizi. Most of
the collections occurred between the 1940s and 1970s
(Fig. 1A) and seasonally between June and August (Fig.
1B), although many records did not include either the
year or month of collection.
Distribution and Habitat
Tretanorhinus 1s a genus exclusive to Middle and South
America, and the West Indies. 7retanorhinus variabilis
is the only one of the species with an unambiguous
distribution, inhabiting Cuba, Isla de la Juventud (Isle of
Youth), and the Cayman Islands (Fig. 2). Tretanorhinus
nigroluteus has been frequently recorded along the
Atlantic coast from southern Mexico to Colombia,
including some islands such as the Bay Islands of
Honduras and Great Corn Island of Nicaragua (Fig.
2). However, records of this species in Colombia are
controversial. Alarcon-Pardo (1978) reported finding 7.
nigroluteus on the Atlantic coast of Colombia, but we
were unable to locate any specimens of this species in
the scientific collections consulted which matched the
locality mentioned by that author. We found only one
specimen of 7! nigroluteus from the Pacific coast of
Colombia as a disjunct point of the species range (Table
1). The distributions of 7. mocquardi and T. taeniatus
are the least clear among the species of the genus.
Tretanorhinus mocquardi ranges from the Canal Zone
in Panama through the Pacific coast of Colombia and
Ecuador, although it has been reported from only two
locations in Colombia and one in Ecuador (Fig. 2, Table
1). Tretanorhinus taeniatus could be endemic to Ecuador
(Table 1), despite previous reports of this species in
Colombia (Castafio-M. et al. 2004; Daniel 1949). Based
on these distributions, 7? mocquardi and T. taeniatus
could be sympatric in Esmeraldas province, northwestern
Ecuador, whereas 7? mocquardi and T: nigroluteus seem
to be sympatric in Choco department on the Pacific coast
of Colombia (Fig. 2).
Most information on the preferred habitat of the
genus comes from studies conducted on 7! nigroluteus
and T. variabilis. Tretanorhinus 1s a fully aquatic genus,
inhabiting all kinds of fresh and brackish water bodies
such as rivers, streams, lagoons, estuaries, mangroves
(Cisneros-Heredia 2005; Neill 1958; Villa 1970), and
even cow wells (Seidel and Franz 1994). The species
require a muddy or rocky bottom with aquatic vegetation
where they can hide and rest (Neill 1965; Villa 1970).
Although there are reports of individuals found out of
the water (e.g., crossing roads), these events occur after
flooding that forces the snakes to search for another water
body (Barquero et al. 2005; Villa 1970). The distributions
of 7. nigroluteus and T. variabilis also confirm the ability
of these snakes to disperse and survive in salt water
(Barbour and Amaral 1924: Neill 1958), since they have
colonized several islands. In that regard, we observed
December 2019 | Volume 13 | Number 2 | e208
Barquero and Arguedas
Species
© mocquarai
nigroluteus
@ faeniatus
variabiis
QO 200 400 800 1,200 1,600
a es KT
Fig. 2. Map showing the current distribution of the four species of Zretanorhinus based on specimens from scientific collections.
Table 1. Number of specimens of Tretanorhinus species collected from different countries and held in several scientific collections.
Specimens with a doubtful or missing location were excluded (n = 38).
Country T. mocquardi T. nigroluteus T. taeniatus T. variabilis Total
West Indies
Cayman Islands - - - 58 58
Cuba - - - 280 280
Middle America
Belize - 52 - - 52
Costa Rica - 11 - - 11
Guatemala - 11 - - 11
Honduras - 157 - - 157
Mexico - 30 - - 30
Nicaragua - 65 - - 65
Panama 14 19 - - 33
South America
Colombia 4 1 - - 5
Ecuador 6 - 9 - 15
Total 24 346 9 338 717
Amphib. Reptile Conserv. 229 December 2019 | Volume 13 | Number 2 | e208
Biology of Tretanorhinus species
Table 2. Morphological information available in the literature for each species of Tretanorhinus.
Trait T. mocquardi T. nigroluteus T. taeniatus T. variabilis
SVL (mm)
Adults - 242-656 440 500-800
Juveniles - 140-168 - 143-145
Tail length (mm)
Adults - 142-206 130 145-160
Juveniles - 51-77 ~ -
No. of loreals 1 1-2 1 1-3
No. of prefrontals 1-2 2 3 )
No. of preoculars 2 2-3 2 1-3
No. of postoculars - 2 2 2
No. of temporals - 1+2 BE? 243 1+2
No. of upper labials - 7-9 8 8-9
No. of lower labials - 9-12 4—5 9-11
No. of ventrals 166-177 127-151 168-175 152-168
No. of caudals 69-85 56-81 74-81 48-81
Posterior chin-shields In contact In contact Separated Separated
No. of dorsal rows 19 19, 21 21 1D: 2)
Ventral color Fuliginous yellow rane. eee yellow, - ae dats
Ventral pattern -
Dorsal color Ss
3 longitudinal
Dorsal pattern ;
stripes
an individual of 7) nigroluteus resting on a beach on
the Caribbean coast of Costa Rica after a heavy rain,
suggesting that the snake had been washed out to sea,
surviving until it was returned to land by the tide.
Morphology
Morphological information is limited and incomplete
for TZ] mocquardi and T: taeniatus, despite both species
being described more than 110 yrs ago by Bocourt
(1891) and Boulenger (1903), respectively. Table 2
provides a summary of some morphological features
that were extracted from the literature review. Overall,
Tretanorhinus are relatively small snakes; 7. variabilis is
the largest species with an SVL of up to 800 mm. All four
species in the genus exhibit a grayish dorsal coloration
with stripes, spots, or bands, and a yellow, orange, or
gray ventral coloration. Juveniles have been found in
the wild only infrequently, and the sex of most collected
individuals was not identified (Table 3). Juveniles of
each species resemble the adults in pattern and coloration
(Barquero et al. 2005; Petzold 1967).
Amphib. Reptile Conserv.
With or without dots or spots
Olive, grayish brown, light
brown, black
With or without dark spots
3 dark stripes Light dots or spots
Grayish olive, dark
Grayish olive Beaten
3 longitudinal
: Blackish cross bands
stripes
Previous attempts to produce a key to the species
of the genus have never included all four species.
Therefore, the following key is presented to unify the
previous efforts (Bocourt 1891; Boulenger 1893; Dunn
1939; Peters and Orejas-Miranda 1970; Kohler 2008)
and incorporate more recent data.
Key to the species of 7retanorhinus:
la. Dorsum without stripes, more than one loreal can be
present. «7.2. 8.4.. BONE Shley ie
1b. Dorsum: with three longitudinal stipes. only one Joreal
2a. Posterior chin-shields in contact, ventrals fewer than
152. Focad ae nigroluteus
2b. Posionet chinshields ‘Separated ‘wenthals 152 or
more. He. ots eke, VALLADALS
3a. Less ‘than three ptefrontals. posterior chin- shields in
contact.. ay : ..mocquardi
3b. Three preftontals, posterior chin-shields separated
..taeniatus
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Barquero and Arguedas
Taxonomy and Systematics
The evolutionary relationships of the genus are enigmatic
and controversial, so that 7retanorhinus has been placed
within different former subfamilies of Colubridae (e.g.,
Natricinae, Xenodontinae, and Dipsadinae) by various
authors (Crother 1999; Dowling et al. 1996; Pinou and
Dowling 1994; Villa 1969). The general consensus 1s that
the genus should be placed within Dipsadidae (formerly
Dipsadinae, Grazziotin et al. 2012; Pinou and Dowling
1994) and it is commonly referred to as a xenodontine
(Cadle 1985; Minton 1976; Vidal et al. 2000). Moreover,
the phylogenetic relationships with other genera are still
ambiguous. Crother (1999) placed Tretanorhinus as the
sister taxon of Sibon or the Sibon-Manolepis clade. In
two studies that included more taxa, Grazziotin et al.
(2012) noted that Tretanorhinus could be the sister taxon
of Hypsiglena, and both genera were placed in a clade
containing 7rimetopon, Geophis, and Atractus, whereas
Pyron et al. (2013) placed Tretanorhinus as the sister
taxon of the Leptodeira-Imantodes clade. However, in all
these studies the relationships of Tretanorhinus with other
taxa were poorly supported and the genus is considered as
Dipsadidae incertae sedis (Grazziotin et al. 2012).
The affinities of each species within Tretanorhinus
are also enigmatic, and this is caused by the lack of
information on the basic biological aspects of some
species. Detailed morphological information is only
available for 7. nigroluteus and T. variabilis (Table 2). No
author has given a complete morphological description
of 7’ mocquardi, such that even basic phenotypic traits
(e.g., most head scutellation and dorsal coloration)
are missing (Table 2). In the case of 7 taeniatus,
morphological information has only been reported for
females, as males have never been deposited or identified
as such in scientific collections (Table 3). Despite these
deficiencies, morphological information compiled from
the literature review here suggests that 7. taeniatus and 7:
mocquardi are more closely related to each other than to
7. nigroluteus and T: variabilis.
Problems have also arisen with the subspecies
described for both TZ nigroluteus (dichromaticus,
lateralis, mertensi, nigroluteus, and obscurus) and T.
variabilis (binghami, insulaepinorum, lewisi, variabilis,
and wag/eri). The morphological variables used to define
the subspecies have been chosen arbitrarily (Wilson
and Hahn 1973). For example, differences in coloration
have been used by some authors to differentiate among
subspecies with only superficial descriptions (Schwartz
and Ogren 1956; Smith 1965; Villa 1969). In addition,
no genetic analyses have yet been reported to confirm the
validity of these subspecies.
Ecology and Natural History
Information on the ecology and natural history of 7.
mocquardi and T. taeniatus is virtually non-existent
Amphib. Reptile Conserv.
Table 3. Number of specimens of Tretanorhinus held in
scientific collections that have been identified as female, male,
or juvenile.
Species Female Male Juvenile Total
T. mocquardi 2 1 - S)
T. nigroluteus 14 16 2 32
T. taeniatus 2 - - 2
T: variabilis 19 17 4 40
Total 37 34 6 77
and they remain poorly studied for 7. nigroluteus and T.-
variabilis. Snakes of Tretanorhinus are nocturnal and seem
to hide during the day in water bodies amongst roots and
rock crevices (Barbour and Ramsden 1919; Stuart 1937;
Villa 1970). Some unusual features have been identified
for the genus. For example, individuals of Tretanorhinus
feed upon fishes, tadpoles, and frogs by either actively
chasing prey or remaining motionless with the tail and
body attached to a supporting surface (e.g., branch or rock)
and striking at passing prey (Barquero et al. 2005; Neill
1965; Petzold 1967; Wilson and Hahn 1973). In addition,
these snakes demonstrate shy behavior, such as fleeing to
the bottom of water bodies when disturbed (Stuart 1937)
and rolling up the body like a ball when caught (Petzold
1967; Seidel and Franz 1994). Known natural predators
of Zretanorhinus include, but are probably not limited
to, turtles (e.g., Kinosternon [Villa 1973]) and wading
birds (e.g., Tigrissoma and Cochlearius [Villa 1970]).
A specimen from Costa Rica was collected from a crab,
thus confirming the assumption of Villa (1970) that some
species of crabs can be predators of Tretanorhinus.
Information on reproduction is scarce for all four
species of Tretanorhinus, although observations in
captivity demonstrate that 7’ nigroluteus and T: variabilis
are oviparous, laying 6—9 adherent eggs out of water
(Barquero et al. 2005; Petzold 1967). Tretanorhinus
variabilis lays larger eggs (35[L] x 16.75[W] mm on
average) that hatch earlier (35 d) than 7) nigroluteus
(21.5[L] x 10[W] mm, 42 d). Villa (1970) found gravid
females of 7. nigroluteus during both the dry and wet
seasons, suggesting that reproduction could occur
year-round in this species. Most gravid females of 7°
variabilis have been found during the wet season in July
and August (Petzold 1967; Seidel and Franz 1994). Both
T! nigroluteus and T. variabilis are sexually dimorphic,
with females being larger than males and only males
possessing tubercles on scales of the head (Henderson
and Hoevers 1979; Petzold 1967).
The capacity to survive in salt water likely contributed
to the colonization of Caribbean islands and northeastern
South America from a Central American ancestor
(Cisneros-Heredia 2005; Hedges 1996) and allowed 7.
nigroluteus and T! variabilis to become fairly abundant in
some parts of their ranges (Henderson and Hoevers 1977;
Schwartz and Henderson 1991). Henderson and Hoevers
(1977) reported that 7. nigroluteus was more frequently
December 2019 | Volume 13 | Number 2 | e208
Biology of Tretanorhinus species
found during the dry season (December to May) than
during the wet season (June to November) of Belize,
a difference explained by the overflowing of the river
system studied. However, historical collections of this
species show that more individuals have been collected
during the wet season, a pattern shared with T. variabilis
(Fig. 1), and in accordance with reports by Wilson and
Hahn (1973) for Roatan Island, Honduras. 7retanorhinus
mocquardi and T: taeniatus are less abundant than the
other two species and no pattern of variation in abundance
can be elucidated from available data.
General Considerations and Future Research
This study has summarized information about the
species of the genus Tretanorhinus published from
1854 (Dumeril et al. 1854) to the present (Estrella-
Morales and Piedra-Castro 2018). Information was also
incorporated on all collected specimens of this genus that
could be identified as preserved in scientific collections
throughout the world. This integrative approach allowed
the identification of gaps in our knowledge about these
snakes. For example, it is surprising that (1) a complete
morphological description is not available in the literature
for 7’ mocquardi, (2) only a few specimens have been
collected for 77] mocquardi and T. taeniatus, and (3) most
natural history and ecological information simply has
never been reported for any of the species. In addition
to the lack of key data, much available information is
contradictory, such as the reported occurrence of 7
nigroluteus and T: taeniatus in Colombia, which can
cause several problems. Therefore, one can ask how a
reliable identification of individuals in the field can
be made when such basic data are missing. This is
particularly problematic for sympatric species, such as
7. nigroluteus and T: mocquardi in Panama, and for 7:
mocquardi and T: taeniatus in Ecuador.
In order to fill in the gaps in our knowledge of
Tretanorhinus, future research should focus on at least
three areas. First, validation of the currently accepted
species and subspecies 1s absolutely urgent. Barbour
and Amaral (1924) have questioned the validity of 7.
mocquardi (although see Dunn 1939), while Wilson and
Hahn (1973) refused to recognize 7: n. dichromaticus.
Therefore, a comparative study of all species and
subspecies that includes both morphological and genetic
data and produces a phylogeny of the genus is necessary.
Previous attempts have failed to include all species or
have used only morphological or genetic data. Second,
both field and lab studies are needed to increase our
knowledge about these secretive and, in some areas,
elusive species. Tretanorhinus mocquardi and T.
taeniatus require extensive work on morphological
variation, ecological habits, distribution patterns, and
natural history traits. Breeding behavior is completely
unknown for these two species and males of 7) taeniatus
have yet to be measured and described. Although
Amphib. Reptile Conserv.
there is significantly more information available for 7:
nigroluteus and 7: variabilis, nothing is known about
their courtship, sexual selection, development, and
many other aspects of basic biology. Third, demographic
variation and population dynamics need to be quantified
to understand the movement of individuals among
populations, sex ratios, and population sizes. These types
of data are essential for determining the conservation
status of species. Some efforts have already been made
to identify areas of high and low abundance across the
ranges of 7: nigroluteus and T: variabilis. However, long-
term studies which monitor changes in populations are
yet to be done.
The problems mentioned above are not restricted only
to Tretanorhinus species, as they also apply to many other
snakes (Dorcas and Willson 2009), and it is alarming
that we rely so heavily on unconfirmed or erroneous
information. Snakes in particular require special attention
due to the intrinsic difficulties in generating accurate
information. These difficulties arise from certain aspects
of their biology, including low densities, great mobility,
and cryptic habits. Integrative studies, such as this one,
are important for identifying the gaps in our knowledge
of different taxa and guiding future efforts in the right
direction.
Acknowledgements.—We are grateful to all the curators
at institutions that kindly provided us with the information
on specimens of 7retanorhinus. We are also thankful to
Pablo Allen, Guido Saborio, and Rowan McGinley for
their helpful comments on the manuscript.
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December 2019 | Volume 13 | Number 2 | e208
Biology of Tretanorhinus species
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Marco D. Barquero is a Costa Rican biologist with a Doctorate degree from Macquarie
University, Sydney, Australia. Marco has dedicated the last 18 years to the study of amphibians
and reptiles in different parts of the world, but especially in Costa Rica.
Viviana Arguedas is a Costa Rican biologist with a Master’s degree from the University of Costa
Rica. Viviana has studied different taxa over the last 14 years, with an emphasis on herpetofauna.
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Francis, London, United Kingdom. 504 p.
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Amphib. Reptile Conserv. 234 December 2019 | Volume 13 | Number 2 | e208
12,
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42.
Barquero and Arguedas
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comments on the phylogeny of some mainland xenodontines. Contemporary Herpetology 2: 7-30.
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Museum, Biological Sciences 17. 93-150.
86. Wood GC. 1939. The genus 7retanorhinus in Cuba and the Isle of Pines. Proceedings of the New England Zo6élogical
87.
Club 18: 5-11.
Zaher H; de Oliveira L; Grazziotin FG; Campagner M; Jared C; Antoniazzi MM; Prudente AL. 2014. Consuming
viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary
Biology 14: 58-86.
Amphib. Reptile Conserv. 237 December 2019 | Volume 13 | Number 2 | e208
Appendix 2. Number of specimens of 7retanorhinus held in each scientific collection from which data were obtained.
Specimens Abbrev
7 ANSP
143 AMNH
1 BYU
59 CAS
12 CM
8, CHP
12 FMNH
82 FLMNH
6 FHGO
12 INHS
5 IBUNAM
8 IAvH
35 LACM
64 LSUMZ
45 MPM
15 MNHN
60 MCZ
3 MVZ
By USNM
1] BMNH
5 RBINS
3 ROM
3 TCWC
vs MHUA
12 MZUCR
2 UVC
1 UTCH
2 UCM
77 KU
10 UMMZ
4 UTA
7355 Total
Amphib. Reptile Conserv.
Biology of Tretanorhinus species
Institution name
Academy of Natural Sciences, Philadelphia
American Museum of Natural History
Bingham Young University, Monte L. Bean Life Science Museum
California Academy of Sciences
Carnegie Museum of Natural History
Circulo Herpetologico de Panama
Field Museum of Natural History
Florida Museum of Natural History
Fundacion Herpetologica Gustavo Orcés
Illinois Natural History Survey, University of Illinois (formerly University of
Illinois Museum of Natural History [UIMNH])
Instituto de Biologia, Universidad Nacional Autonoma de México
Instituto de Investigacion de Recursos Biologicos Alexander von Humboldt
Los Angeles County Museum of Natural History
Louisiana Museum of Natural History (formerly Louisiana State University,
Museum of Zoology)
Milwaukee Public Museum
Muséum National d’ Histoire Naturelle
Museum of Comparative Zoology, Harvard University
Museum of Vertebrate Zoology, University of California at Berkeley
National Museum of Natural History, Smithsonian Institution (formerly United
States National Museum)
Natural History Museum (formerly British Museum of Natural History)
Royal Belgian Institute of Natural Sciences
Royal Ontario Museum
Texas Cooperative Wildlife Collection
Universidad de Antioquia, Museo de Herpetologia
Universidad de Costa Rica, Museo de Zoologia
Universidad del Valle
Universidad Tecnologica del Choco
University of Colorado, Museum of Natural History
University of Kansas, Biodiversity Institute
University of Michigan, Museum of Zoology
University of Texas at Arlington
238 December 2019 | Volume 13 | Number 2 | e208
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 239-258 (e209).
urn:lsid:zoobank.org:pub:7751CF14-97D4-4874-88CE-5567ED7B72AF
Three new species of Hemidactylus Oken, 1817
(Squamata, Gekkonidae) from Iran
'2:3Farhang Torki
'Razi Drug Research Center, Iran University of Medical Sciences, Tehran, IRAN *FTEHCR (Farhang Torki Ecology and Herpetology Center for
Research), 68319-16589, P. O. Box: 68315-139 Nourabad City, Lorestan Province, IRAN *Biomatical Center for Researches (BMCR), Khalifa,
Nourabad, Lorestan, IRAN
Abstract.—Based on morphological characters, three new species of the genus Hemidactylus are described,
one from the Zagros Mountains (Khuzestan Province) and two from the coastal Persian Gulf (Bushehr Province)
of Iran. The three new species can be differentiated from all other Hemidactylus inhabitants of Iran and adjacent
area congeners by distinct morphometric, meristic, and color characters. Comparisons with other species of
Hemidactylus are presented and a key to the genus is provided. Some information about the ecology, biology,
and conservation of the three new species is provided. Existing data suggest these geckos are point endemics.
Some additional historical information about the Hemidactylus inhabitants of Iran is discussed, particularly H.
parkeri.
Keywords. Bushehr, Hemidactylus achaemenidicus sp.n., H. pseudoromeshkanicus sp.n., H. sassanidianus sp.n., H.
parkeri, Khuzestan, Sauria, Reptilia
Citation: Torki F. 2019. Three new species of Hemidactylus Oken, 1817 (Squamata, Gekkonidae) from Iran. Amphibian & Reptile Conservation 13(2)
[General Section]: 239-258 (e209).
Copyright: © 2019 Torki. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 In-
ternational (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows:
official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 4 February 2019; Accepted: 20 June 2019; Published: 14 December 2019
Introduction
Globally, the gekkonid genus Hemidactylus Oken, 1817
currently consists of 154 species distributed across all
tropical and subtropical continental landmasses, including
intervening oceanic and continental islands (Carranza
and Arnold 2012; Smid et al. 2013a,b, 2015; Uetz 2019).
Four families and 70 species of geckos occur in Iran:
50 species of Gekkonidae, 10 species Phyllodactylidae,
seven species of Sphaerodactylidae, and three species
of Eublepharidae (Uetz 2019). The four Hemidactylus
species reported so far from Iran are: H. flaviviridis, H.
persicus, H. robustus, and H. romeshkanicus (Anderson
1999; Bauer et al. 2006a; Rastegar-Pouyani et al. 2006;
Torki et al. 2011; Kamali 2013; Smid et al. 2014). Only
one of them is endemic to Iran (H. romeshkanicus).
During a 2007-2010 collection program in south-
western Iran, from the Zagros Mountains and coastal
Persian Gulf, several geckos were collected which, upon
laboratory examination, were found to differ in important
characters from Iranian geckos already known.
In this article, they are described morphologically
and compared to the previously known Hemidactylus
species from Iran, as well as those from neighboring
Correspondence. torki,f@iums.ac.ir, torkifarhang@yahoo.com
Amphib. Reptile Conserv.
regions. Additionally, two notes regarding H. parkeri are
presented, and comments on the conservation of geckos
in Iran are provided.
Materials and Methods
During several field trips in the Iranian plateau, three
new Hemidactylus species were collected from this
region (Fig. 1): (a) Kangan region, near the coastal
Persian Gulf, Bushehr province, (b) Tangestan region,
Bushehr province, and (c) Kole-Saat, Khuzestan
province. All specimens of the three new species were
assigned catalog numbers for the ZFMK (Zoologisches
Forschungsmuseum Alexander Koenig, Bonn,
Germany); and FTHM (Farhang Torki Herpetological
Museum, Nourabad City, Iran), with the latter deposited
in Farhang Torki Ecology and Herpetology Center for
Research (FTEHCR).
The taxonomic characters of Hemidactylus species
from Iran are not well defined. For most species, no
museum specimens were available for comparison.
Rather, published descriptions of geckos known from
Iran were compared to the morphological characters of
the newly collected material (e.g., Moravec et al. 2011;
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
Andimeshk
Fig. 1. Type localities of three new geckos in Iran.
Carranza and Amold 2012; Smid et al. 2013a, 2015).
For comparison with H. romeshkanicus ZMB 75020
from the Museum fiir Naturkunde, Leibniz Institut fur
Biodiversitats- und Evolutionsforschung zu _ Berlin
(formerly Zoologisches Museum Berlin, Germany) was
used. For comparison with Hemidactylus spp. distributed
outside Iran, original descriptions or other publications
containing morphological analyses of Hemidactylus
species were used (e.g., Anderson 1999; Giri et al. 2003;
Baha el Din 2003, 2005; Bauer et al. 2006a,b, 2007;
Sindaco et al. 2007; Giri and Bauer 2008; Giri 2008;
Mahony 2010; Agarwal et al. 2011; Busais and Joger
2011; Moravec et al. 2011; Torki et al. 2011; Mirza and
Rajesh 2014; Vasconcelos and Carranza 2014; Carranza
and Arnold 2012; Smid et al. 2013a, 2015; Safaei-
Mahroo et al. 2017).
Characters were selected to optimize comparisons
with data reported by Moravec et al. (2011), Carranza
and Arnold (2012), Wagner et al. (2014), Vasconcelos
and Carranza (2014), and Smid et al. (2013a, 2015).
Measurements were taken using a dial caliper with 0.01
mm precision. Additionally, other characters important
for the taxonomy of Hemidactylus were used, such
as nasals in contact and 1“ postmental in contact with
2™ lower labial (e.g., Moravec et al. 2011; Smid et
al. 2013). Characters used to describe the three new
Hemidactylus are as follows: SVL: snout-vent length;
TRL: trunk length; TL: tail length; Rl: TL/SVL; HL:
head length; HW: head width; HH: head height; R2: HL/
Amphib. Reptile Conserv.
(H. pseudoromeshkanicus sp.n.)
, lange stan (H. sassanidianus sp.n.)
Kangan (H. achaemenidicus sp.n.)
SVL; R3: HW/HL; R4: HH/HL; OD: orbital diameter;
NE: nares to eye distance; IN: internarial distance; IOI:
anterior interorbital distance; [02: posterior interorbital
distance; TB: longitudinal tubercle rows; PAP: number
of precloacal pores; SL (L/R): number of supralabials; IL
(L/R): number of infralabial scales; LP1 (L/R): number
of lamellae under the first finger of the pes; LP4 (L/R):
number of lamellae under the fourth finger of the pes; FP:
femoral pores; and PM: postmentals. Abbreviations used
in tables are as follows: M: male; F: female; T: total; A:
ANOVA test; F: one-way ANOVA F value; dF: degrees
of freedom; P: probability; DM: Difference of means;
and DD: Direction of difference.
Because of the absence of sexual size dimorphism
in the arid clade of Hemidactylus (Carranza and Arnold
2012), both sexes were analyzed together. Statistical
procedures used to test for differences between the sexes
included one-way ANOVA (at 95% confidence level [P <
0.05]) and Principal Component Analysis (PCA).
Taxonomy
Hemidactylus achaemenidicus sp.n. (Figs. 2—5)
Hemidactylus turcicus - Torki et al. 2011
Hemidactylus persicus - Carranza and Arnold 2012
Hemidactylus persicus - Smid et al. 2013
urn: sid: zoobank.org:act:40139EE0-898A-4E3B-B9B7-32C73 FE 16377
December 2019 | Volume 13 | Number 2 | e209
Fig. 2. Dorsal and ventral views of (a, b) holotype and (ce, d)
paratype specimens of Hemidactylus achaemenidicus sp.n.
Holotype
ZFMK 98567, adult male, collected at the end of the southern
Zagros Mountains, Kangan, Bushehr Province, Southern
Tran, on 10 May 2008 (27°18’N, 52°42’E, 50-221 m asl).
Paratypes
ZFMK 97750-97753; ZFMK 98568—-73; and FTHM
005110, six adult male specimens (ZFMK 97750-97752;
ZFMK 98569-—70; FTHM 005110), and four adult female
specimens (ZFMK 97753; ZFMK 98568, 71, 72), same
data as for holotype.
Diagnosis
A small sized Hemidactylus, maximum snout-vent
length 39.8 mm; tubercles distributed over the entire
dorsum (except for forelimbs); granules cover head and
extend to neck; tubercle rugosity dimorphism occurs
between males and females over dorsal body, limbs, and
tail (males have more rugose tubercles than females):
proximal portion of tail (ventral view) covered by small
scales without femoral pores; precloacal pores present;
six tubercles on most whorls of tail; two postmentals; low
number of lamellae under pes; subcaudal scales started
more distally (approximately after proximal one-third of
tail), only a few subcaudals (plate-like) in original tail
(O—22), that started so far as anal; proximal dorsal tail
covered by regular whorls of tubercles (keeled in male
and plate-like in female); ventral scales not imbricate; the
ends of ventral scales are denticulated; enlarged scansors
beneath fingers, scansors are mostly divided, terminal
scansor is single; dorsal color pattern shows much
variability (regular or irregular crossbars, longitudinal
bands, large or small spots), and this is true for the tail
(regular or irregular bars, large and small spots), venters
of all specimens are without spots (uniform).
Description of Holotype (Figs. 2—3)
Measurements (in mm): body size: 39.8; tail length: 40.5;
interlimbs: 18.3; head width: 7.3; head length: 11.7; head
depth: 4.9; eye-eye: 4.7; ear opening: 0.82; eye diameter:
3.0; forelimb length: 12.3; hindlimb length: 15.5.
Amphib. Reptile Conserv.
Fig. 3. (a) Postmentals and (b) precloacal pores in holotype of
Hemidactylus achaemenidicus sp.n.
Body depressed, tail more or less flattened; head
triangular-shaped; two postmentals, 1 postmentals
enlarged and in contact, 2" postmentals behind the first
enlarged postmentals, the 1“ postmentals in contact
with the 1% infralabials, the 2" left postmental distinct
from infralabials by one series of scales, the 2" right
postmentals in contact with the 2™ infralabials (and
weakly with the 1*), four scales between 2™ postmentals;
Infralabials: eight; supralabials: nine; nostril surrounded
by five scales (the 1“ supralabial, rostral, three small on
posterior); nasals not in contact and separated by one
scale; ear openings more or less falcate-shaped, and
horizontal; 14 scales between nostril and eye; 24 scales
between eye and ear; rostrum covered by large granules;
space between eyes covered by 27 small granules, and
10 small simple tubercles distributed among them; upper
head covered by smallest granules and many small simple
tubercles distributed among them; tubercles on upper ears
and behind eyes are simple; tubercles on occiput mostly
simple and less pointed; tubercles on neck are pointed
and keeled (heterogeneous); from rostrum to neck body
covered by granules; tubercles distributed on dorsum,
head, and limbs; tubercles not found on arm; most body
tubercles are keeled; dorsal tubercles are strongly keeled,
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
Fig. 4. Subcaudal of tail of (a) ZFMK97753 and (b) ZFMK 98567 of He
between (c) holotype of H. achaemenidicus sp.n. and (d) lectotype of H. robustus. Photo from Smid et al. 2015.
tubercles on proximal of back surrounded by 11-12
scales (middle: 12-13, distal: 13), dorsal tubercles do
not show regular form and abnormalities occur in a few
points (intermixed with some small simple tubercles);
enlarged, trihedral, and strongly keeled tubercles
distributed on distal part of dorsum (between hindlimbs)
as well as nearest to tail; tubercles on forearm are simple;
tubercles on femur heterogeneous (simple, pointed, and
keeled); foreleg tubercles heterogeneous in size and
shape (pointed and keeled); size of the tubercles on limbs
is different and is as follows: foreleg > femur > forearm;
scales on palm and sole are granule-like; 17 rows (mostly
regular) of tubercles on back; 21 tubercles between
interlimbs.
Tail is original; first part of tail (one-third) covered
by small scales, subcaudal plates cover following third,
less than 12 scales (moderate size: 50% of tail width, not
imbricate) on subcaudal, last part; distal one-third of tail
is without subcaudals (covered by small scales); without
crossbars on dorsum of tail, small irregular spots present
in first half of tail; tubercle whorls only found on first
half of tail, 1‘ to 6" whorls more or less irregular and
separated by one scale, includes six large, trihedral, and
strongly keeled tubercles, after them real whorls start:
six tubercles in 1* to 3 whorl, four for 4" to 7", first
whorl separated from secondary by two scales, four
scales between 2"*-3" and 34". six scales between 4°—
5". five between 5-6" and 6"—7"| after them tubercles
converted to scales; seven (3+1+3) precloacal pores; no
femoral pores; enlarged scansors are plate-like; terminal
scansor is single; lamellae on fingers as follows: 1*: five,
2": seven, 3™: seven, 4": seven, 5": eight; lamellae on
pes as follows: 1%: six, 2": eight, 3: nine, 4": 10, 5%:
eight; claws in front of scansors. Palm and sole covered
by granule-like scales.
Coloration of upper head is covered by longitudinal
discontinuous rows that extended to neck, and are
Amphib. Reptile Conserv.
\
irregular onto dorsal body; dorsum without bars; few
irregular bars and small spots cover dorsum of tail;
one bar between nostril-eye-ear; venter of body, limbs,
and tail uniformly without pattern; pattern in preserved
specimen is similar to the live specimen and all spots and
bars are obvious; the preserved specimen is colorless.
Variation (Fig. 4a—b)
Some variation among paratypes 1s described as follows:
tubercles distributed all over dorsum (except arms);
granules cover head and extend to neck. Tubercle
rugosity differed between males and females on overall
dorsal body, limbs, and tail (males with more strongly
rugose tubercles than females), females have wide
(approximately flattened shape) dorsal tubercles and
males have extended trihedral tubercles. Proximal tail
in most specimens is cycloid and ventral view covered
by small scales (same as dorsum); proximal tail (dorsal
view) covered by 4-6 irregular whorls of tubercles
(strongly keeled) separated by one scale, followed by
regular whorls of six tubercles in each whorl, started and
separated by 2-6 scales, more than six regular whorls are
obvious in all specimens (first half) and do not continue
to posterior half of tail (tubercles converted to scales).
Number of precloacal pores is variable as follows: six (five
Specimens), seven (holotype), and eight (ZFMK97751).
Most specimens have two postmentals, postmentals in all
specimens are not uniform and variability is as follows:
one specimen (ZFMK 98570) has five postmentals
(left+right), two anterior, two posterior, and one large
scale between anteriors; anteriors not in contact with
one another and in contact with 1% and 2" infralabials;
seven specimens have normal postmentals and anterior
in all specimens in contact with 1* and 2" infralabials; in
one specimen (FTHM005110) 2" postmentals (left and
right) separated from infralabials by one series of scales,
and 1‘ postmentals in contact with 1* infralabial; left 2"
December 2019 | Volume 13 | Number 2 | e209
midactylus achaemenidicus sp.n. Comparison of dorsal body
Torki
Fig. 5. Type locality of Hemidactylus achaemenidicus sp.n.,
Kangan, Bushehr, southern Iran.
postmental in ZFMK97751 separated from infralabials
by one series of scales, and 1‘ postmentals are in contact
with 1* infralabials; finally left 1‘ postmental of ZFMK
98571 contacts 1* infralabials. Subcaudal scales begin
approximately after first third of tail, a lesser number
of subcaudals (plate like) in original tail (0 to 22); first
half of dorsal tail covered by regular whorls of tubercles
(strongly keeled in males and plate-like in females).
Dorsal color pattern is variable (regular or irregular cross
bars, longitudinal band, large or small spots), this is true
for tail (regular or irregular bars, large and small spots),
venter of all specimens is uniform, without spots; venter
in live specimens is white and tail is yellowish or dark,
in preserved specimens ventral is yellowish and ventral
of tail is darkish. More data on the variation are shown
in Table 1.
Sexual dimorphism is evident. In general, males show
larger body size and head size than females (Table 1).
Amphib. Reptile Conserv.
Based on statistical analysis three characters, TRL, [O2,
and LPAR, are significantly different between the sexes
as follows: males have significantly (P = 0.03, f = 6.21)
larger trunk length than females (16.9 + 0.37 vs. 14.3 +
1.28); this is true for IO2 and in males (4.70 + 0.1) is
significantly (P = 0.03, f = 6.09) larger than in females
(4.22 + 0.18). In contrast, number of lamellae under 4"
pes (right side) in females (10 + 0.0) is significantly (P
= 0.01, f = 8.18) greater than in males (9.28 + 0.18).
Five characters (SVL, TRL, TL, HW, HL) in females
show much more variability than in males; in contrast,
three characters (OD, NE, IN) in males are much more
variable than in females. All females have 16 dorsal
tubercle rows, and in males they number 16 or 17 (16.4 +
0.2). Lamellar variability under 1‘ and 4" finger of pes in
females is zero and in males is one (except ILL: female
is one and males are zero). More data on the dimorphism
are shown in Table 1.
Habitat and Ecology (Fig. 5)
Hemidactylus achaemenidicus sp.n. are distributed in the
eastern part of Bushehr Province (edge of Hormozgan
Province), in Kangan, Assaloye City. The habitat of H.
achaemenidicus sp.n. is flat land covered by Jujube trees
(Ziziphus jujuba). The type locality is located in the
northern part of the Persian Gulf. A few lizard and snake
Species were observed at the type locality: 7rapelus
agilis, Laudakia nupta, and Echis carinatus.
Distribution
So far, the species is only known from the type locality.
Etymology
The species name “achaemenidicus” refers to “The
Achaemenid Empire,” also called the First Persian
Empire. It was an empire based in Western Asia, founded
by Cyrus the Great, and notable for including various
civilizations and becoming the largest empire at that
time.
Comparisons
Based on a phylogenetic study of one paratype specimen
(FTHM 005100 is erroneous and FTHM 005110 is the
true code; also the locality cited in the phylogeny section
must be changed to the type locality of the new species)
H. achaemenidicus sp.n. is completely distinct from
H. robustus, H. turcicus, and other recently described
species inhabiting Oman (see phylogram of Carranza
and Arnold 2012; Smid et al. 2015). Hemidactylus
achaemenidicus sp.n. was compared with the re-
description of H. robustus Smid et al. (2015) [see Table
2]. Hemidactylus achaemenidicus sp.n. is different from
H. robustus by smaller body size in males (36.5 + 0.9 mm
vs. 41.8 + 2.3) and females (33.1 + 2.0 mm vs. 43.6 +
4.7), more longitudinal tubercle rows (16.2 + 0.1 vs. 14.8
+ 1.2), and keeled (vs. weakly keeled and posteriorly
pointed) as well as rugosity dimorphism (quite distinct
December 2019 | Volume 13 | Number 2 | e209
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December 2019 | Volume 13 | Number 2 | e209
244
Amphib. Reptile Conserv.
Table 2. Comparison three new Hemidactylus species with other Hemidactylus which occur in Iran. Data from: (1): Carranza and Arnold
Torki
2012; (2): Torki et al. 2011; (3): FTHM collections. Abbreviation are as given in Materials and Methods and Table 1 header.
Characters § H. achaemenidicus sp.n. H. sassanidianus sp.n. —_H.. pseudoromeshkanicus spn. _—_-H.. persicus (1) H. romeshkanicus (2) H. flaviviridis (3)
SVL 28-39 48-63 74-75 36-67 70 59-79
TL 24-41 66-79 88 55-77 83 60-97
SL 9-10 10-13 11 10-13 15 12-17
IL 7-8 8-10 9 8-11 9 11-12
HL 8.7-12.2 13.5-20.6 22.8-23.4 9.1-16.8 23.2 17-23
HW 5.4-7.5 9.7-13 14.6-15.2 7.1-14.4 14.5 12.5-18.5
HH 3.7-5.3 6.1-8.9 8.7-9.1 4.9-9.6 9.1 7.9-10.9
HL/SVL 0.27-0.31 0.28-0.31 0.30-0.31 0.21-0.28 0.33 0.28-0.31
HW/HL 0.60—-0.68 0.60-0.71 0.64—0.65 0.67-0.92 0.62 0.65-0.80
HH/HL 0.39-0.47 0.35-0.45 0.37-0.40 0.42-0.60 0.39 0.40-0.48
DTR 16-17 14-16 16-17 14-16 16 -
PAP 6-8 6-8 12 8-11 12 -
LPI 5-6 6-9 11 8-9 8 8-9
LP4 9-10 9-14 15 13-14 12 11-13
PM 2 2-4 2 2 3 2
for new Hemidactylus species), subcaudal scales (scale
like and/or enlarged vs. enlarged), less head width/head
length (0.62 vs. 0.74), internarial distance (0.97 + 0.04
vs. 1.5 + 0.08), lower number of lamellae under the 1“
pes (5.7 + 0.1 vs. 6.1 + 0.5), internarial distance (0.97 vs.
1.5), and nasal in contact % (0% vs. 22%) [Carranza and
Arnold 2012; Smid et al. 2015]. Based on photograph of
lectotype of H. robustus (Figs. 4-9 in Smid et al. 2015;
as a female specimen), females of H. robustus have
approximately full rugosity (lectotype of H. robustus is
female) and it is more than in male H. achaemenidicus
sp.n. (males of H. achaemenidicus sp.n. have much
greater rugosity than females); dorsal tubercle density
(especially on proximal part) in H. robustus 1s more than
H. achaemenidicus sp.n. dorsal, and dorsolaterals of
H. robustus have maximum uniformity; in contrast the
dorsum of H. achaemenidicus sp.n. has heterogeneity
of dorsal and dorsolateral tubercles; also shape and size
of tubercles on dorsolateral of H. achaemenidicus sp.n.
is different from mid-dorsum, in contrast to H. robustus
(Fig. 4c—d); photographic comparison: limbs (especially
hind limbs) in H. achaemenidicus sp.n. are smaller than
H. robustus, additional differences are: longer head for
H. robustus; smaller interlimbs for H. robustus, base
of tail in H. robustus is much more flattened and in H.
achaemenidicus sp.n. is approximately cylindrical.
Differs from H. flaviviridis, H. persicus, and H.
romeshkanicus by smaller body size. More comparisons
with Hemidactylus inhabiting Iran are shown in Table 2.
Differs from H. turcicus by smaller body size (36.5 + 0.9
mm vs. 46.0 + 5.8 in males, 33.1 + 2.0 mm vs. 49.2 +
5.1 in females), short tail relative to SVL (TL 0.98 vs.
112.8% of SVL), more longitudinal tubercle rows (16.2
+ 0.1 vs. 13.8 + 0.7), nasal in contact % (0% vs. 13.3%),
1s' and 2" postmentals in contact with 2" infralabials
(81.8% vs. 12.9%), lower number of lamellae under the
1* pes (5.7 vs. 6.6), supralabials (9.5 + 0.1 vs. 8.3 + 0.5),
infralabials (7.8 + 0.1 vs. 6.8 + 0.4), number of precloacal
pores (6.42 vs. 7.2), less head width/head length (0.62 vs.
Amphib. Reptile Conserv.
0.77) [Moravec et al. 2011; Smid et al. 2013]. Different
from H. persicus in body size, tail length, head shape
and ratio, dorsal tubercle rows, precloacal pores, and
number of lamellae under the 1% and 4" pes (see Table
2). Different from H. romeshkanicus in body size, tail
length, head shape, precloacal pores, and number of
lamellae under the 1‘t and 4" pes (see Table 2).
In this section H. achaemenidicus sp.n. is briefly
compared with other Hemidactylus spp. from Iran. Different
from H. adensis, H. awashensis, H. lavadeserticus, H.
mandebensis, H. ulii, and H. jumailiae by more longitudinal
tubercle rows (16.27 vs. 14, 14, 14, 13.3, 14.1, and 14)
[Smid et al. 2013a, 2015]. Different from H. dawudazraqi
by more dorsal tubercle rows (16-17 vs. 12-15). Different
from H. alfarraji by precloacal pores (6-8 vs. 4) [Smid et
al. 2016]. Different from H. kurdicus by postmentals (2 vs.
1) [Safaei-Mahroo et al. 2017]. Different from H. foudaii
by precloacal pores (6-8 vs. 9) and well developed dorsal
and tail tubercles (vs. less developed and protuberant
dorsal and particularly tail tubercles). Different from
H. mindiae (Jordan) and H. asirensis by smaller body
size (36.5 mm vs. 49.3, 43-48.5 in males, 33.1 mm vs.
49.8, 38-51 in females, respectively) [Baha el Din 2005,
Moravec et al. 2011; Smid et al 2017]. Different from H.
saba, H. granosus, H. yerburii, H. montanus, H. minutus,
H. homoeolepis, and H. mindiae (Egypt population) by
number of precloacal pores (6.42 vs. 8, 5.6, 13.7, 11.2, 5.8,
4.3, 12.8, and 4) [Baha el Din 2005; Carranza and Arnold
2012: Smid et al. 2013a, 2016; Vasconcelos and Carranza
2014], respectively. Different from H. endophis by
lacking femoral pores. Different from H. shihraensis, H.
hajarensis, H. luqueorum, H. festivus, and H. alkiyumii by
smaller body size. Significantly different from H. mindiae,
H. lavadeserticus, H. dawudazragi, H. shugraensis, and
H. sinaitus by small body size and more dorsal tubercle
rows. Different from H. leschenaultii, H. homoeolepis,
H.. paucituberculatus, H. inexpectatus, H. masirahensis,
and H. /emurinus by having large and keeled tubercles on
dorsal body.
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
=
m,
Fig. 6. Dorsal tubercles of (a) holotype and (b) paratype of
Hemidactylus sassanidianus sp.n.
Based on recent a molecular study on Hemidactylus
(Maximum-likelihood tree inferred using 350 bp of
the 12S gene, Appendix HI, by Carranza and Arnold
2012; Smid et al. 2013b, 2015), H. achaemenidicus
sp.n. (FTHMO005110 is the accurate specimen number)
is significantly different from: H. /uqueorum, H.
hajarensis, H. lemurinus, H. yerburii, H. montanus,
H. jumailiae, H. alkiyumii, H. robustus, H. sinaitus, H.
saba, H. shihraensis, H. festivus, H. paucituberculatus,
H. masirahensis, H. inexpectatus, and H. homoeolepis.
Hemidactylus sassanidianus sp.n. (Figs. 6—9)
Hemidactylus persicus Torki et al. (2011)
urn:Isid:zoobank.org:act:61 CDBB8A-CE1 F-4219-8F66-9DB6275C577E
Holotype
ZFMK 98573, adult male, collected at the southern end
of Zagros Mountains, Khaiiz, Tangestan City, Bushehr
Province, Southern Iran, on 4 May 2008 (28°43’N,
51°31’E, 525 m asl).
Paratypes
ZFMK 97754—-56, ZFMK 98574—77, FTHM 005029;
four adult male specimens (ZFMK 97756, ZFMK
98575-77), and four adult female specimens (ZFMK
Amphib. Reptile Conserv.
97754—55, ZFMK 98574, FTHM 005029), same data as
for holotype.
Diagnosis
A small-sized Hemidactylus, snout-vent length at
least 48.3 mm; tubercles distributed all over dorsum,
except for arm; back with enlarged keeled tubercles;
heterogeneity of dorsal tubercles occurred in all
specimens (a few parts or most of dorsal body);
dorsal scales in a few places converted into granules;
granules cover snout, between eyes, upper head, neck,
and in some specimens onto middle of dorsum and
dorsolaterals; 2—4 postmentals; 4-8 whorls of tubercles
on first half of dorsum of tail, distal part of tail without
tubercles; without femoral pores; precloacal pores
present; more lamellae under fingers; subcaudal
scales enlarged; ventral scales not imbricate; enlarged
scansors beneath fingers, scansors mostly divided,
terminal scansor single; limbs without color pattern
and uniform, dorsolaterals without any pattern and
uniform, pattern only present on middle part of dorsum
(longitudinal) of all specimens, various patterns on
dorsum such as: spotty (small or large), bars (irregular
and regular); ventrum without pattern.
Description of Holotype (Fig. 6)
Measurements (in mm): body size: 54.2; tail length:
79.3; interlimbs: 21.6; head width: 10.6; head length:
16.4; head depth: 6.4; eye-eye: 6.2; ear opening: 1.9; eye
diameter: 4.3; forelimbs length: 18.3; hind limbs length:
24.8.
Body depressed; body, as well head are flattened; tail
flattened; head triangular-shaped; two postmentals, the
first postmentals are enlarged and are widely in contact
together, the 2"! postmentals one behind the first enlarged
postmentals, the 1‘ postmentals are in contact with the
1st infralabials, the 2™ postmentals are in contact with
the 2"! infralabials, four scales between 2™ postmentals;
infralabials: nine; supralabials: left: 11, right: 12; nostril
surrounded by five scales (the 1% supralabial, rostral,
internasal scale and two postlabials); nasals not in contact
and separated by one small scale; ear openings are falcate-
shaped, and horizontal; 14 scales between nostril and eye;
26 scales between eye and ear; 31 scales between eyes;
rostrum covered by large granules and a few tubercles
distributed in distal part; between eyes covered by small
granules, and nine small smooth and simple tubercles
distributed among them; upper head covered by smallest
granules and small tubercles distributed among them;
tubercles on upper ears simple and pointed; tubercles
on occipital are mostly pointed; tubercles on neck are
simple, pointed and keeled (heterogeneous); granules
cover rostrum to neck body; tubercles distributed on
dorsum, head, and limbs; tubercles extend to in front of
eyes; tubercles not found on arm; most body tubercles are
keeled; dorsal tubercles are keeled, a few areas of mid-
dorsum covered by abnormal tubercles (heterogeneous in
December 2019 | Volume 13 | Number 2 | e209
Torki
Fig. Te Postmental variation in Hemidactylus SETTER
sp.n. (a) ZFMK 98573; (b) FTHM 005029; (c) ZFMK 97756;
(d) ZFMK 98575.
shape and type) and granules; dorsolateral tubercles are
keeled and wide; forearm tubercles are small and simple;
size of the forearm tubercles are smaller than hindlimb
tubercles; number of tubercles on femur (pointed and
keeled) are less than foreleg (mostly keeled); scales on
palm and sole are granular; 16 regular rows of tubercles
on back; 6—8 small simple tubercles between interorbits,
32 scales between interorbits (mid-part); 22 enlarged
tubercles between fore- and hindlimbs; 12-14 scales
surround each mid-dorsal tubercle (11-12 proximally,
12-13 distally); 3-4 scales between each dorsal tubercle.
Tail is original; 52 enlarged imbricate subcaudal
scales; last part of tail cycloid-shape and covered
by raised scales; proximal of tail covered by several
continuous indistinct bars, 13 crossbars on dorsum of
tail, tubercle whorls only found in anterior part of tail,
5—6 scales between each whorl, six tubercles in first
whorl, six tubercles in the second, six in third, five in
fourth, five in fifth, six in sixth, and six tubercles in the
seventh whorl, after the seventh whorl tubercles become
very small (six in each whorl) and converted into scales;
ventral scales (mostly oval shape) are not imbricate and
their size in the middle part of the body are larger than
other regions; eight (4+4) precloacal pores; without
femoral pores; enlarged scansors are plate-like, terminal
scansor 1S unique (not paired); lamellae on fingers as
follows: 1‘: nine (1-3 undivided), 2": 10 (1 undivided),
3 10 (1 undivided), 4: 11, 5%: 11(1-2 undivided);
lamellae on pes as follows: 1%: nine (1-2 undivided),
2™: 11 (1 undivided), 3": 12 (1 undivided), 4": 14 (1-2
undivided), 5": 13; palm and sole covered by granule-
like scales.
Coloration: upper head, neck, and middle part of
dorsum covered by smallest spots and few large paled
spots (background view), don’t form bar; without spots
or bars on dorsolaterals and limbs; one narrow stripe
between nostril-eye and eye-ear; three moderate spots
on snout; a paled and irregular bar on occipital and neck;
Amphib. Reptile Conserv.
he y f ‘iit “Y J
ey wot 9 Le ee #35 is
ety ‘ } ie 2, tp ry a
Fig. 8. (a) Precloacal pores (ZFMK 98573), and (b) dorsal
tubercles (ZFMK 98573) of Hemidactylus sassanidianus sp.n.
color of venter is uniform white; palm of digits (hindlimbs
and forelimbs) more or less white; pattern of preserved
Specimen is similar to the live specimen, but has lost color.
Variation (Figs. 7-8)
Heterogeneity of dorsal tubercles occurs in a few areas,
mostly on the dorsal body; tubercles converted to simple
(not-keeled) and have abnormal shape (e.g., rounded,
width, semi), in these parts most dorsal scales converted to
granules (small or large); granules cover snout and extend
to upper head and neck (all specimens), or onto proximal
dorsum (ZFMK 97754 and 28) or onto mid-dorsum
(ZFMK 97755), lateral sides of neck strongly covered by
granules and tubercles (ZFMK 97756); most specimens
have 1—2 tubercles in front of ear, or 4-5 (ZFMK 98573
and ZFMK 97756) or lack tubercles (ZFMK 98577);
internasals in four specimens are in contact (ZFMK
98573, ZFMK 98575, ZFMK 97754—55) and in others
separated by one (ZFMK 97756, FTHM005029), two
(ZFMK 98577) or three (ZFMK 98574) scales; number
of postmentals is variable (usually two) between 2-4,
asymmetry occurs in some of them; ZFMK 98575 have
four PM as follows: 1‘ PM is large and in contact with
1st and 2™ infralabials, 2" PM on posterior of 1** PM and
in contact with 2™ infralabials, 3" PM behind 2"? PM
and separated from infralabials by one series of scales;
4‘t PM in contact with 1‘ and 2™ postmentals; ZFMK
97756 has three postmentals as follows: 1* larger and in
contact with 1* and 2™ infralabials, 2" PM is behind 1*
PM and in contact with 2" infralabials, 3" PM is behind
2™ PM and separated from infralabials by one series of
scales, 10 scales between 2" postmentals; FTHM005029
has three PM on left and two on right; ZFMK 98574
has three PM on left and two on right; 4-8 whorls of
tubercles on proximal half of dorsum of tail (usually
six), without tubercles on distal part of tail; limbs and
December 2019 | Volume 13 | Number 2 | e209
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December 2019 | Volume 13 | Number 2 | e209
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Amphib. Reptile Conserv.
=
dorsolaterals are uniformly without pattern, pattern only
present on middle part of dorsum (longitudinal) of all
specimens, various patterns are visible on dorsum such
as: spots (small or large), bars (irregular and regular);
ZFMK 98574: 1% bar is full and wide, 2"! as well as 3%
are X-shaped, and usually 4" bar as well; ZFMK 98575:
narrow longitudinal stripe on middle part of dorsum,
two bars (usually X-shaped) on neck; FTHM005029:
six bars on dorsum, five regular and one irregular, one
irregular bar on neck; FTHM005029: one longitudinal
stripe from neck to tail; upper head and between eyes of
most specimens covered by small spots. More data on the
variations are shown in Table 3.
Sexual dimorphism is evident. In general, 12
characters are larger in females and 11 characters larger
in males. Females (26.5 + 0.74) have significantly (P =
0.01, f = 9.59) larger trunk length than males (22.8 +
0.87), as the result of fecundity selection (e.g., Andersson
1994; Torki 2012), and females have a larger trunk for
the development of two large eggs. The lamellae in
females (1%: 9; 4%: 13.7) number more than in males
(1s: 8; 4%: 12.2), which may be the result of natural
selection, because during development of the two large
eggs females must have more ability to move (Torki
2012); also, females have minimal variability of number
of lamellae (1%: 0; 4: 1) in contrast to males (1: 3; 4":
5); greater number lamellae and minimal variability in
females are important positive results of natural selection
for survival of H. sassanidianus sp.n. under natural
conditions (personal assumption of author). In general,
all characters (except dorsal tubercles rows), especially
body size (range: males: 15; females: 2.9) have more
variability in males. More data on the dimorphism and
variability are shown in Table 3.
Habitat and Ecology (Fig. 9)
The Tangestan region is at the end of the southern part of
the Zagros Mountains, and has palm trees. Hemidactylus
Sassanidianus sp.n. is distributed in a mountainous
area. This mountain is one of the Zagros Mountains
and its structure is sedimentary. Shelter sites of the
new Hemidactylus species are limited to the clefts and
Amphib. Reptile Conserv.
Fig. 9. Type locality of Hemidactylus sassanidianus Sp.n., Tangestan, Bushehr, southern Iran.
ot
en.
meet
.-
a :
+
gre
od
Me
caves in this mountain, with many specimens found and
collected in one cave in this locality. This cave is deep—
the author was able to reach a depth of more than 50 m,
though the depth of this cave is said to be even more
than 200 m. This cave is an important habitat for this
new Hemidactylus and the largest population was seen
only in this cave. Other species of gecko were also seen
in this cave, such as Asaccus tangestanensis. Of the three
new species described here, only H. sassanidianus sp.n.
was seen in this cave, but H. sassanidianus sp.n. was not
seen outside of the cave or elsewhere in the entire region.
This cave probably opens into other regions, and further
investigation of this cave is needed. This cave is dark
during both day and night. Conditions inside the cave are
moist, in contrast to the conditions outside the cave.
Distribution
Hemidactylus sassanidianus sp.n. is distributed only
at the type locality, in Khaiiz, Tangestan City, Bushehr
Province, southern Iran. The type locality is situated at
the end of the southern Zagros Mountains, approximately
150 km from the Persian Gulf.
Sympatric Lizards and Snakes
Several lizard and snake species were observed in
the type locality, including Asaccus tangestanensis,
Laudakia nupta, Trapelus agilis, Tropiocolotes persicus,
Coluber (sensu lato) sp., Macrovipera lebetina, and
Echis carinatus.
Etymology
The species name “sassanidianus” refers to “The
Sasanian Empire,” also known as Sassanian, Sasanid,
Sassanid or Neo-Persian Empire, which was known to its
inhabitants as Eranshahr in the Middle Persian language.
Comparisons
Hemidactylus sassanidianus sp.n. differs from H.
persicus (based on original description by Anderon
1872) by: (1) Dorsal tubercles in H. sassanidianus sp.n.
are not strongly keeled and in some parts tubercles are
not keeled, in contrast they are strongly keeled in H.
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
Table 4. Sexual dimorphism among Hemidactylus persicus, H. sassanidianus sp.n., and H. achaemenidicus sp.n. Abbreviations:
HL: head length; HW: head width; HH: head height; IO1: anterior interorbital distance; [O02: posterior interorbital distance; SL:
number of supralabial; IL: number of infralabial scales (all data are means). F: female, M: male, sig: significant (Carranza and
AE:
rae ar
ae Ce
001
ee ee ce
0.29
Arnold 2012).
H. persicus
H. sassanidianus sp.n.
H. achaemenidicus sp.n.
persicus. (2) Heterogeneity of dorsal tubercles occurred
in all specimens of H. sassanidianus sp.n., in contrast to
original description of H. persicus. (3) Size of tubercles
in H. sassanidianus sp.n. is smaller than H. persicus,
about 0.4 of ear opening vs. 0.5 ear opening. (4) Five or
six tubercles in each row of the tail in H. sassanidianus
sp.n., and in contrast H. persicus have seven tubercles in
each row of the tail. (5) Dorsal body of H. sassanidianus
sp.n. covered by spots (not bars), in contrast dorsal body
in H. persicus is covered by transverse narrow band.
More differences between H. sassanidianus sp.n. and
H. persicus (based on original description and Anderson
1999): (6) H. persicus only has two postmentals (in all
populations; there are no records in the literature), in
contrast H. sassanidianus sp.n. has 2—4 postmentals.
(7) In Anderson’s work on H. persicus inhabiting Iran,
he reported 9-11 preanal pores, which is clearly more
than H. sassanidianus sp.n. (6-8). (8) Tail sharp in
H. sassanidianus sp.n., and not sharp in H. persicus.
Additional differences with H. persicus include:
number of postmentals (2-4 vs. 2), mental trihedral (vs.
pentagonal); relatively fewer precloacal pores in males
(6-8 vs. 9-11); number of lamellae under the first digit
of the pes (6—9 vs. 8-9); body size of H. sassanidianus
sp.n. males (54.7) smaller than females (56.4), this is in
contrast to H. persicus (males: 59; females: 51.4); head
longer (HL/SVL: 0.3 vs. 0.24), elongated (HW/HL:
0.64 vs. 0.8), and more flattened (HH/HL: 0.4 vs. 0.49)
[Carranza and Arnold 2012]; sexual dimorphism in head
size (HL, HW, and HD) occurs for H. persicus (males
significantly larger than females), this is in contrast to H.
sassanidianus sp.n., and this is true for more characters
(Table 4). Easily differentiated from H. romeshkanicus by
number of precloacal pores (6-8 vs. 12), other differences:
smaller body size, number of supralabials, and dorsal
tubercle shape (not trihedral vs. enlarged trihedral). It is
different from H. robustus by larger body size in both
sexes combined (48-63 vs. 32—50) and in males (54.7 vs.
41.8) and females (56.4 vs. 43.6); more lamellae under
Amphib. Reptile Conserv.
M
rie | as
Pras [3s
029 |
ee ee M
the 1% (8.5 vs. 6.1) and 4" (12.8 vs. 10.1) digits of the
pes; more supralabials (11.8 vs. 9.4); and greater number
of precloacal pores (7.4 vs. 6.1) [Carranza and Arnold
2012: Smid et al. 2013a, 2015] (Table 2). Different from
H. achaemenidicus sp.n. by larger body size (48-63 vs.
28-39), tail, dorsal tubercle rows, number of lamellae
under digits of pes, labials, and postmentals (see Table
2). Different from H. flaviviridis by presence of dorsal
tubercles and without femoral pores. More comparisons
are shown in Table 2
In this section H. sassanidianus sp.n. is_ briefly
compared with other Hemidactylus species outside of
Iran. Different from H. dawudazragi and H. shihraensis
by body size (48-63 vs. 40-49 and less than 49,
respectively). Different from H. asirensis by larger body
size (48.3-63.3 mm vs. 43-48.5 in males, 54.5—57.4
mm vs. 38.3—51.1 in females) and HL/SVL (28-31%
vs. 23-28%). Different from H. alfarraji by precloacal
pores (6-8 vs. 4) [Smid et al. 2016]. Different from H.
kurdicus by postmentals (24 vs. 1) [Safaei-Mahroo et
al. 2017]. Different from H. lavadeserticus by enlarged
keeled tubercles on back (vs. not so enlarged). Different
from H. foudaii by precloacal pores (6-8 vs. 9) and well
developed dorsal and tail tubercles (vs. less developed
and protuberant dorsal, and particularly, tail tubercles).
Different from H. homoeolepis, H. masirahensis, and H.
paucituberculatus by having keeled tubercles on dorsum
(vs. without tubercles on dorsum). Different from H.
inexpectatus, H. endophis, H. hajarensis, H. yerburii,
H. shugraensis, H. yerburii yerburii, H. montanus, H.
awashensis H. minutus, H. homoeolepis, H. mindiae,
H. lemurinus, and H. granosus by number of precloacal
pores (6-8 vs. 4, 14, 4-6, 12.8, 5, 13.7, 11.2, 4.5, 5.8, 4.3,
4, 6, 5.6, respectively) [Smid et al. 2013a, 2015, 2016;
Vasconcelos and Carranza 2014; Carranza and Arnold
2012]. Different from H. /uqueorum and H. homoeolepis
by body size (55.4 vs. 76.8, 31.8) [Carranza and Arnold
2012]. Different from H. turcicus by postmentals (2-4
vs. 2), more longitudinal tubercles on dorsum (15.5 vs.
December 2019 | Volume 13 | Number 2 | e209
c [ek er i
pbs aay aye ts Per id aae fest Raper * > i
ee a aS Le &
Fig. 10. Dorsal and ventral view of (a, b) holoty
13.8), more lamellae under the 1% (8.5 vs. 6.5) and 4"
(12.8 vs. 9.7) digits of the pes, and more supralabials (11.8
vs. 8.2) and infralabials (8.6 vs. 6.7) [Smid et al. 2013a].
Different from H. sinaitus by larger body size in males
(54.7 vs. 39.5) and females (56.4 vs. 45.6), more lamellae
under the 1% (8.5 vs. 5.7) and 4" (12.8 vs. 9.7) digits of
the pes, and more supralabials (11.8 vs. 8.7) [Carranza
and Arnold 2012]. Different from H. jumailiae by more
supralabials (11.8 vs. 9.8), more lamellae under the 1 (8.5
vs. 6.9) and 4" (12.8 vs. 10.9) digits of the pes (Smid et
al. 2013a). Different from H. festivus, H. alkiyumii, and
H. saba by more longitudinal tubercles on dorsum (15.5
vs. 13.3, 12.9, 14) [Smid et al. 2013a; Carranza and
Armold 2012]. Different from H. ulii, H. mandebensis,
and H. adensis by larger body size in males (54.7 vs. 38.6,
41.5, 34) and females (56.4 vs. 40.1, 35, 36.7), and more
longitudinal tubercles on dorsum (15.5 vs. 14.1, 13.3,
aes
Amphib. Reptile Conserv.
ZFMK 97757
aes fies ss
i oa,
: i ere ee a
pe and (c,d) paratype sp cimens of H. pseudoromeshkanicus sp.n.
14) [Smid et al. 2013]. Different from H. /emurinus, H.
masirahensis, H. inexpectatus, H. paucituberculatus,
H. homoeolepis, H. leschenaultii, and H. flaviviridis by
having numerous enlarged tubercles on upper surface of
body (vs. no enlarged tubercles on upper surface of body).
Hemidactylus pseudoromeshkanicus sp.n. (Figs. 10—
12)
urn: Isid:zoobank.org:act: ACECB18C-9C39-4270-A404-BCD88DFCAA52
Holotype
ZFMK 98578, adult male, collected on the western
slope of central Zagros Mountains, Kole-Saat region
Andimeshk, Khuzestan Province, western Iran on 14
June 2010 (32°52’N, 48°43’E, altitude 607 m asl) by
Farhang Torki.
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
Fig. 11. Comparison of postmentals (PM). (a) Three well developed PM in H. romeshkanicus (Holotype, ZMB 75020) and (b) two
postmentals of H. pseudoromeshkanicus sp.n. (Paratype, ZFMK 97757).
Paratype
ZFMK 97757, adult female, same data as for holotype.
Diagnosis
A medium sized Hemidactylus, snout-vent length at
least 74 mm; tubercles distributed all over the dorsum
(except for arms); back with enlarged trihedral keeled
tubercles; granules (rather than scales) cover head and
extend to neck, and rarely to forelimbs; without femoral
pores; precloacal pores present; tubercular heterogeneity
present on dorsum (proximal and distal parts), limbs,
neck, head, and dorsolateral; six tubercles in all whorls
of tail; two postmentals; more lamellae under fingers;
subcaudal scale enlarged; ventral scales not imbricate,
and the ends of ventral scales are simple (cycloid at mid-
part; weakly denticulate at distal and proximal parts of
ventral); enlarged scansors beneath fingers, scansors are
mostly divided, terminal scansor is single; intermixed
color pattern on dorsal body; sexual dichromatism (in
both dorsal and ventral body) occurs between male
(holotype) and female (paratype).
Description of Holotype (Fig. 10a—b)
Measurements (in mm): body size: 75.2; tail length:
88.7; interlimbs: 30.8; head width: 15.2; head length:
23.4: head depth: 8.7; eye-eye: 8.8; ear opening: 3.2; eye
diameter: 5.4; forelimbs length: 29.9; hind limbs length:
33:3.
Body depressed; body, as well as head flattened:
tail more or less flattened; head triangular-shaped; two
postmentals, the first postmentals are enlarged and are
in contact, the 2" postmentals behind the 1‘ enlarged
postmentals; the 1 postmentals are in contact with the
1*t infralabials, the 2"¢ postmentals are in contact with
the 1* and the 2" infralabials, nine scales between 2™
postmentals; infralabials: nine; supralabials: 11; nostril
surrounded by five scales (the 1* infralabial, rostral,
three postnasals); nasals not in contact and separated
by one small scale; ear openings are falcate-shaped,
Amphib. Reptile Conserv.
and horizontal; 19 scales between nostril and eye; 20
scales between eye and ear; rostrum covered by large
granules; between eyes covered by small granules, and
small tubercles (simple and rarely pointed) distributed
among them; upper head covered by smallest granules
and small pointed tubercles distributed among them;
tubercles above ears pointed; tubercles on occipital
mostly pointed and less keeled (heterogeneous);
tubercles on neck pointed and keeled (heterogeneous);
from rostrum to neck covered by granules; tubercles
distributed on dorsum, head, and limbs; tubercles not
found on arms; most body tubercles are keeled; dorsal
tubercles are enlarged, mostly trihedral and strongly
keeled, some of them pointed especially between limbs
(cross view); keeled tubercles between hindlimbs (cross
view: proximal dorsum) intermixed with small and
moderate pointed tubercles, tubercles heterogeneous
(small, large, keeled, pointed, simple) obvious on distal
dorsum (near tail); tubercles on femur mostly trihedral
and keeled (mostly scale-like, different from tubercles on
dorsum); tubercles on forearm are keeled (scale-shape,
different shape from tubercles on dorsum), pointed
and simple (heterogeneous in size and shape); size of
the forearm tubercles smaller than hindlimb tubercles;
scales on palm and sole are granule-like; 16 regular rows
of tubercles on back; 11—13 small tubercles (simple or
pointed) between interorbits; 23 enlarged interlimb
tubercles; 16-17 scales surround each dorsal tubercle;
4—S scales between dorsal tubercles; tail is original; 53
enlarged imbricate scales on subcaudal; last part of tail
cycloid-shape and covered by raised scales; 22 crossbars
on dorsum of tail, 1-3 crossbars are irregular and other
crossbars are regular; tubercle whorls only found in first
part of tail, five scales between each whorl, six tubercles
in 1% whorl, six tubercles in the 2", six tubercles in 3",
and six tubercles in the 4" whorl, after the 5“ whorl
tubercles become very small (six in each whorl); ventral
scales are not imbricate and their size at mid-body are
larger than in other regions, the ends of ventral scales are
December 2019 | Volume 13 | Number 2 | e209
Torki
Fig. 12. Type locality of H. pseudoromeshkanicus sp.n. in
Kole-Saat, Andimeshk, Khuzestan province.
simple (mostly cycloid, not denticulate); 12 precloacal
pores; without any femoral pores; enlarged scansors are
plate-like, terminal scansor is unique (not paired); 1‘
scansor in most fingers 1s unique; lamellae on fingers as
follows: 1s: 11 (1-3 undivided), 2": 11, 3°: 12, 4: 13,
5: 13 (1-3 undivided); lamellae on pes as follows: 1*:
11 (1-3 undivided), 24: 12, 3": 13, 4%: 15, 5": 15; claws
in front of scansors; palm and sole covered by granule-
like scales.
Coloration: irregular grayish pattern covers most of
dorsum extending onto dorsolaterals; occipital covered
by one spotted-bar that extends into eyes; snout is light
grayish; neck region covered by one great grayish spotted-
bar; forearm covered by small gray spots; hindlimbs
covered by light irregular bars that are in contact with
one another; proximal tail covered by irregular bars that
are in contact together, black bars cover distal tail; arm
is without spots; dorsal view of hindlimb digits darker
than forelimb digits; chin is yellowish and light red; color
of ventrum more or less yellowish, without any spots or
bars; palms of digits (hindlimbs and forelimbs) are ashy.
Pattern 1s similar to the live specimen and all spots and
bars are obvious in preserved specimens; the preserved
specimen is colorless.
Description of Paratype (Figs. 2c—d, 11b)
Measurements (in mm): body size: 74.2; tail length: not
original; interlimbs: 31.7; head width: 14.6; head length:
22.8: head depth: 9.1; eye-eye: 9.8; ear opening: 3.2; eye
diameter: 5.1; forelimbs length: 27.4; hind limbs length:
32.4.
Most data are similar to holotype, but some small
differences as follows: 11 scales between 2™ postmentals;
between eyes covered by small granules, and small
tubercles (simple, pointed, and rarely keeled) distributed
among them; upper head covered by smallest granules
and small pointed (rarely keeled) tubercles distributed
among them; tubercles on neck are less pointed and
mostly keeled (heterogeneous); 17 regular rows of
tubercles on back; 18 enlarged tubercles between fore-
and hindlimbs; 16-18 scales surround each dorsum
Amphib. Reptile Conserv.
tubercle; tail 1s missing (most part), zigzag form (without
any crossbars), tubercle whorls only found in first part of
tail, six tubercles in all whorls, 6—7 scales between each
whorl, whorl tubercles distinct by 1-3 scales; ventral
scales are not imbricate and their sizes at mid-body are
larger than in other regions, the ends of ventral scales
are simple (cycloid at mid-part; weakly denticulate at
distal and proximal parts of ventral); without precloacal
pores; without any femoral pores; enlarged scansors are
plate-like, terminal scansor is unique (not paired); first
scansors of most fingers are unique; lamellae on fingers
as follows: 1 and 24: 11, 3": 12, 4 and 5": 13; lamellae
on pes as follows: 15: 11, 2": 13, 3%: 14, 4" and 5%: 15.
Color pattern: intermixed irregular (in contact)
black and grayish pattern covers most parts of dorsum
that extend onto dorsolaterals; bar and inter-bar cover
proximal and distal dorsum; an irregular black stripe
extends to eyes; neck region covered by one great black
bar; one narrow black stripe between eyes and nostrils;
one wide black stripe between eye and ear which extends
to occipital region; forearm covered by small gray spots,
hindlimbs covered by irregular bars that are in contact
with one another; tail covered by irregular bars that are
in contact (without crossbar on tail); arm is without
spots; in dorsal view hindlimb digits strongly darker
than forelimb digits; chin is yellowish, color of ventrum
is light, without any spots or bars; palms of digits
(hindlimbs and forelimbs) are white or less ashy. Pattern
is similar to the live specimen and all spots and bands are
obvious in preserved specimen. The preserved specimen
is colorless.
Habitat and Ecology (Fig. 12)
Specimens belonging to Hemidactylus pseudo-
romeshkanicus sp.n. were collected from the Kol-e-Saat
region, Andimeshk, Khuzestan province. Kol-e-Saat
Region is located between Lorestan-Khuzestan Provinces
and has warm climatic conditions; it is located between
the central Zagros Mountains and Khuzestan Plain. Oak
(Quercus brantii) forest is distributed in the mountains
of this region. The new Hemidactylus specimens show
nocturnal activity, and feed on small insects and insect
larvae occurring in the habitat. Individuals of the new
species actively climb on rocks, and specimens were
collected on rocks during the middle of the night.
Distribution
Presently, this new species is only recorded from
the type locality at Kol-e-Saat region, Andimeshk,
Khuzestan Province, Iran. In spite of several field trips
to areas adjacent to the type locality, no specimens
belonging to this new taxon were found. But based on
geomorphological patterns of the folded mountains of the
western slope of Zagros Mountains, the main distribution
of H. pseudoromeshkanicus sp.n. is expected to extend
towards the mountains of northern Khuzestan province.
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
Sympatric Lizards and Snakes
From the type locality the following additional reptile
species were recorded: Asaccus nasrullahi, Cyrtopodion
scabrum, and Pseudocerastes fieldi.
Etymology
The name “pseudoromeshkanicus” is an allusion to its
similarity to H. romeshkanicus. The color pattern of
this new species appears similar to H. romeshkanicus,
but morphological characters do not match this species,
therefore the prefix “pseudo” is used for the new species.
Comparison with Hemidactylus romeshkanicus
Hemidactylus pseudoromeshkanicus sp.n. 1s significantly
different from H. romeshkanicus by several characters as
follows: two postmentals (instead of three developed in
H. romeshkanicus, Fig. 11); H. pseudoromeshkanicus
sp.n. has more lamellae under 4" digit of pes (13 instead
of nine), 1° digit (11 instead of eight), and 4" digit (15
instead of 12) than H. romeshkanicus (which is slightly
true for other fingers); whorl tubercles on tail (number,
size, and arrangement) as follows: number of tubercles
in each whorl in H. pseudoromeshkanicus sp.n. from 1*
to 4" is unique (6-6-6-6), in contrast in H. romeshkanicus
decreasing number of tubercles from 1 ‘to 4" whorl (7-6-5-
4). scales between each whorl in H. pseudoromeshkanicus
sp.n. more than H. romeshkanicus (5—7 instead of
four); supralabials in H. pseudoromeshkanicus sp.n.
significantly less than H. romeshkanicus (11 instead of
15); tubercle rugosity (in general) on dorsum of body of H.
romeshkanicus is stronger than H. pseudoromeshkanicus
sp.n. (one significant example: three views of trihedral
tubercles show rugosity, that rarely occurs for H.
pseudoromeshkanicus sp.n.), tubercular heterogeneity
(small and large trihedral, pointed) occurs on proximal
and distal part of dorsum of H. pseudoromeshkanicus
sp.n., in contrast to H. romeshkanicus. Nasals separated
by one small scale in H. pseudoromeshkanicus sp.n.,
in contrast, one large scale separates nasals in H.
romeshkanicus.
Comparisons with other Hemidactylus
In general, H. pseudoromeshkanicus sp.n. 1s significantly
different from H. robustus, H. persicus, H. sassanidianus
sp.n., and H. achaemenidicus sp.n. by having mostly
enlarged trihedral tubercles on dorsal body. Differs from
H. robustus in body size (than less 50 vs. at least 74
mm) and tail with more precloacal pores (12 vs. 6—8),
tail tuberculation (keeled and raised instead pointed),
and different dorsal color patterns (irregular bands vs.
spotted). Differs from H. persicus by larger body size
and stronger tubercle rugosity on entire dorsal body and
limbs, head shape and size, and dorsal tubercle rows
(Table 2). Differs from H. flaviviridis by having enlarged
tubercles on dorsum, and without femoral pores. For more
comparisons see Table 2. Differs from H. sassanidianus
sp.n. and H. achaemenidicus sp.n. by having more
Amphib. Reptile Conserv.
precloacal pores (12 vs. 6-8, 6—8, respectively), larger
body size, tail with more dorsal tubercle rows, dorsal
tubercle shape and size (more rugosity and larger in size
for H. pseudoromeshkanicus sp.n.), and more lamellae
under fingers (Table 2).
Brief comparisons show differences of H.
pseudoromeshkanicus sp.n. from other Hemidactylus
spp. outside of Iran. Differs from H. dawudazraqdi,
H. hajarensis, H. homoeolepis, H. jumailiae, H.
Shihraensis, H. alfarraji, H. asirensis, and H. foudaii
by precloacal pores (12 vs. 6-8, 4-6, 3-6, 6-9, 6, 4,
6, 8-10, respectively). Differs from H. kurdicus by
postmentals (2 vs. 1) and precloacal pores (12 vs. 10)
[Safaei-Mahroo et al. 2017]. Differs from H. montanus
by more lamellae beneath 4" digit of pes (15 vs. 9-12).
Differs from H. endophis by large body size (74-75
vs. 59), strongly keeled dorsal tubercles (vs. relatively
weakly keeled), and without femoral pores (vs. 14
pores). Differs from H. /emurinus by presence of well-
developed dorsal tubercles (vs. none). Differs from
H. luqueorum, H. festivus, H. paucituberculatus, H.
lavadeserticus, H. masirahensis, and H. inexpectatus
by more precloacal pores (12 vs. 5-6, 6, 6, 6, 4, and 4,
respectively). Differs from H. turcicus by larger body
size and tail, more lamellae beneath 4" digit of pes (13
vs. 8-11), more precloacal pores (12 vs. 6—10), stronger
tubercular rugosity, and different body color patterns.
Differs from H. mindiae, H. granosus, H. mandebensis,
H. awashensis, H. adensis, H. minutus, H. ulii, H. saba,
H. jumailiae, and H. yerburii, by having larger body
size. Differs from H. alkiyumii by having more rows of
tubercles (16-17 vs. 11-14), more lamellae under the 4"
digit of pes (15 vs. 10-12), and more precloacal pores
(12 vs. 6-10). Body size in H. pseudoromeshkanicus
sp.n. is smaller than in H. aaronbaueri, dorsal tubercles
in H. pseudoromeshkanicus sp.n. are much larger than in
H. aaronbaueri, also, color pattern is different from H.
aaronbaueri. By having enlarged, trihedral, and regular
dorsal tubercles H. pseudoromeshkanicus sp.n. is easily
distinguished from several species of Hemidactylus
including: H. aaronbaueri, H. bowringii, H. brookii, H.
flaviviridis, H. garnotii, H. karenorum, H. leschenaultii,
H. maculatus, H. persicus, H. prashad, H. subtriedrus,
and H. triedrus. Digits are relatively slender in H.
scabriceps, but in H. pseudoromeshkanicus sp.n. they
are broadly dilated. H. sinaitus (from Sudan to Northern
Somalia, and Arabia) has smaller and more widely
separated dorsal tubercles, but H. pseudoromeshkanicus
sp.n. has mostly trihedral tubercles.
Note on Hemidactylus Inhabitants from Iran
Hemidactylus inhabitants of the Iranian plateau have a
complicated history. Anderson (1999) reported three
Hemidactylus (H. flaviviridis, H. persicus, and H.
turcicus) from Iran. Anderson (1974) had recorded H.
garnotii in the fauna of Iran, but in 1999 he excluded
254 December 2019 | Volume 13 | Number 2 | e209
Torki
it from Iran due to incomplete data from I. Darevsky;
and he then diagnosed this species as H. flaviviridis
(Anderson 1999). Anderson collected some Hemidactylus
sp. specimens from southwest Iran that do not to match
H. flaviviridis, H. persicus, or H. turcicus (Anderson
1999). Anderson was concerned that H. brookii might
be distributed in southern Iran, but this species has
not been collected inside Iran. Therefore, based on
Anderson’s studies (1999), four species occur in Iran: H.
flaviviridis, H. persicus, H. turcicus, and Hemidactylus
sp. A molecular study (Bauer et al. 2006a) confirmed the
distribution of H. robustus in southwestern Iran; and,
little difference exists between H. robustus from Iran
on the one hand and from the United Arab Emirates and
Egypt on the other. Firouz (2000) has cited H. flaviviridis,
H. persicus, and H. turcicus for the fauna of Iran. Torki
et al. (2011) showed five Hemidactylus species to occur
in Iran, viz: H. flaviviridis, H. persicus, H. turcicus, H.
robustus, and H. romeshkanicus. Due to this author’s
revision of the gecko fauna of Iran (2016-2020 FTE
program), one previous occurrence of Hemidactylus was
identified as H. turcicus (FTHM005100-5110 in Torki et
al. 2011); however, new morphological evidence shows
that it is completely different from H. turcicus as well as
from H. robustus. As described here, this population (H.
achaemenidicus sp.n.) shows differences in important
taxonomic characters from other Hemidactylus species
both inside and outside of Iran (as well as the arid clade).
Hosseinzadeh et al. (2014) worked on the morphology
of Hemidactylus species of Iran, and their work showed
four Hemidactylus species from Iran: H. flaviviridis,
H. persicus, H. robustus, and H. romeshkanicus, as
they rejected H. turcicus from the Iranian gecko fauna.
Based on recent phylogenetic studies on Hemidactylus,
particularly H. turcicus and H. robustus (Carranza and
Arnold 2012; Smid et al. 2013b, 2015), I suggest that
the H. robustus specimens which were examined by
Hosseinzadeh et al. (2014) do match with both H.
turcicus and H. robustus. They do not show the important
taxonomical characters that are important for diagnosis
of H. turcicus and H. robustus from several of those
populations.
Based on recent molecular studies (Carranza and
Arnold 2012; Smid et al. 2013b, 2015), H. persicus
from Iran shows characteristics of being a separate clade
from Arabian Hemidactylus. This clade shows three
distinguishable species, and one of them (FTHM005110)
is the new Hemidactylus achaemenidicus sp.n. described
here. The locality of FTHM005110 cited in_ that
phylogenetic study is incorrect and must be changed to the
type locality of H. achaemenidicus sp.n. given here. On
the other hand, three specimens of H. persicus (JS103—
5) among the Iranian persicus clade (Smid et al. 2013)
showed more differences from other H. persicus, but the
localities of these specimens were not cited in that paper,
and are nearest to the type locality of H. sassanidianus
sp.n. (see Fig. 4 in Smid et al. 2013). On the other hand,
Amphib. Reptile Conserv.
H. robustus from the coastal Persian Gulf (Bandar-e-
Lenge) is a match with the Arabian H. robustus clade
(Smid et al. 2013b, 2015). The oldest reported dispersal
from Arabia occurred 13.1 Ma, when the ancestor of
H. persicus colonized Iran (Smid et al. 2013b). This
time-frame (13.1 Ma) is perfect for speciation among
the Hemidactylus inhabiting the Iranian plateau as well
as the Zagros Fold-Thrust Belt. A few collections from
the southern part of Iran (mostly coastal Persian Gulf)
show three clades in the phylogenetic tree of Smid et al.
(2013b). Based on the distribution of Hemidactylus inside
the Iranian plateau, here I suggest that Hemidactylus has
several monophyletic clades as well as more species
which remain unknown.
Although some works exclude H. turcicus (e.g.,
Hosseinzadeh et al. 2014, Smid et al. 2014) from the
fauna of Iran, Smid et al. (2014) did not explicitly
reject H. turcicus from Iran (see Map 46), and Smid et
al. concluded that H. turcicus 1s not distributed in Iran.
I disagree with those assessments, and do not exclude
this widespread species from the fauna of Iran until more
comprehensive data about the Hemidactylus inhabiting
Iran (especially from phylogenetic studies) are available.
One important reason supporting the acceptability of H.
turcicus for the fauna of the Iranian Plateau is its wide
distribution in adjacent areas to the west (e.g., Turkey)
and east (e.g., Pakistan) of Iran (e.g., Turgay and Atat
1994; Khan 2006).
Bauer et al. (2006a) identified all populations of
small Hemidactylus as a H. robustus. Some authors (e.g.,
Gholamifard and Rastegar-Pouyani 2011; Hosseinzadeh
et al. 2014) followed that assessment. Based on
phylogenetic analysis, H. achaemenidicus sp.n. 1s
completely distinguishable from H. robustus (e.g., Smid
et al. 2013, 2015). Therefore, there are at least three
distinct species of small Hemidactylus in Iran including:
H. robustus, H. turcicus, and H. achaemenidicus sp.n.
Based on all the studies cited above, all Hemidactylus
species of Iran (except H. flaviviridis) show much
complexity and I classify them here in three groups as
follows: H. persicus-complex (including H. persicus, H.
sassanidianus sp.n., and H. achaemenidicus sp.n.); H.
robustus-complex; and H. romeshkanicus-complex (H.
romeshkanicus and H. pseudoromeshkanicus sp.n.).
In summary, at least eight species of Hemidactylus
are distributed on the Iranian Plateau: H. flaviviridis, H.
persicus, H. robustus, H. turcicus, H. romeshkanicus, H.
sassanidianus sp.n., H. achaemenidicus sp.n., and H.
pseudoromeshkanicus sp.n.
Note on Hemidactylus parkeri Loveridge 1936
H. parkeri was described by Loveridge (1936), but this
Species was downgraded or rejected from subsequent
species lists of Hemidactylus (e.g., Arnold 1980; Smid
et al. 2015) and replaced by H. turcicus and H. robustus.
Based on the following reasons, I do not agree with
December 2019 | Volume 13 | Number 2 | e209
Three new Hemidactylus species from Iran
this decision. (i) Type locality: The type locality of H.
parkeri is very far from the type localities of H. turcicus
(Asiatic Turkey, by Moravec et al. 2011) and H. robustus
(“Egypten, Arabien, und Abyssinien” restricted to “the
Red Sea coast of the State of Eritrea” by Smid et al. 2015).
(ii) Ecology and climate: Loveridge (1936) described his
new species in Zanzibar Island (Tanzania), and this island
may have an important role in the speciation of these
geckos. Additionally, Zanzibar Island is located near the
equator, with special ecological and climatic conditions;
and the ecological and climatic conditions of the type
locality of H. parkeri are completely different from the
type localities of H. turcicus and H. robustus. (111) New
methods and insights: Based on phylogenetic studies,
most Hemidactylus species described long ago have been
split into several species, such as H. persicus, H. yerburii,
H. turcicus, and H. robustus (e.g., Carranza and Arnold
2012; Smid et al. 2013, 2015). Therefore, additional
phylogenetic studies on the equatorial Hemidactylus
species are necessary to resolve this problem. (iv) Six
species of Hemidactylus are distributed in Tanzania, and
H. parkeri is not synonymous with all of them (Uetz
2019). On the other hand, only one species is endemic to
Tanzania (H. tanganicus). Based on the above reasons,
there is not a logical and scientific basis for the rejection
of H. parkeri. Therefore, in this study I am in agreement
with Lazza (1978, 1983) on the validity of H. parkeri.
Note on Gecko Conservation in Iran
Based on observations during 20 years, two main threats
for the geckos of Iran are apparent: (1) Rumor: People
in this region believe that geckos are poisonous and fear
them, especially in cities and less so in villages. This
rumor applies to all geckos inhabiting human homes. (11)
Trade: Among geckos, the fat-tailed gecko (Eublepharis)
is an important species that is sold. Eublepharis 1s
considered attractive and some people find it interesting
as a pet. During recent years, trade of this gecko has
increased among the Iranian people. Although 47% of
geckos inhabiting Iran belong to the Red List, the IUCN
category (http://www.iucn.org/) of most is LC (or Least
Concern). The geckos in Iran have the best conservation
situation compared to other amphibians and reptiles, and
their nocturnal activity may have an important role.
Key to Hemidactylus Species Distributed in Iran
la: Dorsal tubercles absent, femoral pores present
LEN ore ne en PL ee ve ee H. flaviviridis
1b: Dorsal tubercles present, femoral pores absent....2
DA IS— Ob. PLEClLOAGAl POFES © FS. Nac 5% glee meow tor azerene 3
2b: 9-11 precloacal pores...........................H. persicus
We Mls preclOacals POLES cat een tate cick Ca Raat 5
3a: 2-4 postmentals, not small Hemidactylus (body
Amphib. Reptile Conserv.
size is more than 48 mm)...... H. sassanidianus sp.n.
3b: Two postmentals, small Hemidactylus (less than 50
4a: Females have less rugosity than males, subcaudals
covered by small scales and/or plate-like scales (few
in number: 0—22)............... H. achaemenidicus sp.n.
4b: Sexual rugosity does not occur (females have
approximately full rugosity), subcaudal scales enlarged
(nopsimalll-seales),, .) 2s. 0/ boda dege o® H. robustus
5a: Two postmentals.....H. pseudoromeshkanicus sp.n.
Sbe Three; postmentals:....of Ree: H.. romeshkanicus
Acknowledgments.—1 wish to thank Professor Steven
Anderson (California, USA) for editing and improving
my manuscript, and Craig Hassapakis (Utah, USA) and
Michael L. Grieneisen (California, USA) for improving
my manuscript. I wish to thank Professor W. Bohme
and his collaborators in ZFMK (ZFMK, Germany) for
marked type specimens.
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Amphib. Reptile Conserv.
Farhang Torki earned his B.Sc. degree in Animal Biology from Lorestan University,
Iran, and his M.Sc. degree in Animal Biosystematics from Razi University in Iran.
During his B.Sc. studies, Farhang worked on histological and embryological methods,
particularly as applied to the spermatogenesis and oogenesis of reptiles, and the herpe-
tofauna of Lorestan Province. During his M.Sc. studies he worked on the systematics
of amphibians and reptiles of the southern and western Iranian Plateau, and continued
his developmental biology work in herpetology. Following his graduate work, Farhang
established (2006) the Farhang Torki Ecology and Herpetology Center for Research
(FTEHCR), the Farhang Torki Herpetology Museum (FTHM), and recently Biomatical
Center for Researches (BMCR) from 2018. Currently, Farhang is studying evolution
and developmental biology, based on mathematical methods. Iran University of Medi-
cal Sciences supported his research during 2018.
258 December 2019 | Volume 13 | Number 2 | e209
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 259-264 (e210).
The Blue Dyeing Poison-Dart Frog, Dendrobates tinctorius
(Dendrobates azureus, Hoogmoed 1969): extant in Suriname
based on a rapid survey
'*Christian A. d’Orgeix, 'De’Jah Hardy, ‘Sarah Melissa Witiak, 7Laren R. Robinson, and *Rawien Jairam
'Department of Biology, Virginia State University, Petersburg, Virginia, 23806, USA *Department of Agriculture and Ecology, Virginia State
University, Petersburg, Virginia 23806, USA *National Zoological Collection of Suriname, Anton de Kom Universiteit, Paramaribo, SURINAME
Abstract.—The blue color morph of Dendrobates tinctorius, originally described as D. azureus, has only been
reported from a few forest islands surrounded by the Sipaliwini savanna in Suriname, South America. The last
published survey of these populations occurred in 1996. The threats of emergent diseases, illegal collecting,
climate change, and habitat destruction through anthropogenic fires toward these populations are unknown.
This report presents the results of a rapid survey of the three forest islands where D. tinctorius historically
occurred to assess its current status. One 50 x 50 m survey plot was established in each of these three forest
islands. A total of 23 frogs were recorded, with some individuals found in each of the forest island surveyed.
These results indicate that D. tinctorius populations are still present at all three historical localities surveyed
by previous researchers in 1968 and again in 1996, although the current surveys found fewer frogs. During the
surveys there was no evidence of illegal collecting or habitat degradation. These observations provide baseline
data that can be used for future monitoring and protection of one of the most geographically restricted and
unique color morphs of D. tinctorius.
Keywords. Amphibia, Dendrobatidae, conservation, Sipaliwini savanna, population decline, habitat fragmentation,
climate change
Citation: d’Orgeix CA, Hardy D, Witiak SM, Robinson LR, Jairam R. 2019. The Blue Dyeing Poison-Dart Frog, Dendrobates tinctorius (Dendrobates
azureus, Hoogmoed 1969): extant in Suriname based on a rapid survey. Amphibian & Reptile Conservation 13(2) [General Section]: 259-264 (e210).
Copyright: © 2019 d’Orgeix et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 10 May 2018; Accepted: 21 February 2019; Published: 18 December 2019
Introduction
The Blue Dyeing Poison-dart Frog was described a
half-century ago as Dendrobates azureus (Hoogmoed,
1969) and subsequently synonymized with D. tinctorius
(Wollenberg et al. 2006). The inclusion of this species
as a color morph of D. tinctorius was also confirmed by
Noonan and Gaucher (2006). Ouboter and Jairam (2012)
considered this species to be a subspecies of D. tincto-
rius due to the geographically isolated occurrence of this
particular morph. Its classification as a subspecies was
refuted by Frost (2017) who maintained this species as
D. tinctorius. Other blue morphs of D. tinctorius were
documented by Silverstone (1975) from Shudikar-wau,
Guyana and by Avila-Pires et al. (2010) from Esta¢ao
Ecolégica Grao-Para North, Brazil. However, specimens
from Suriname do not display the typical light D. tincto-
rius pattern on the dorsum, whereas specimens from the
other mentioned locations still have this pattern.
The predominantly blue color morph (“azureus”) found
in Suriname is restricted to a few isolated “forest islands”
Correspondence. *cdorgeix@vsu.edu
Amphib. Reptile Conserv.
in the Sipaliwini savanna in southern Suriname (Hoog-
moed 1969; Riezebos 1979; Cover 1997; Ouboter and Jai-
ram 2012). This area was mapped in July 1935 when an
expedition by Baron van Lynden was charged with estab-
lishing the southern border of Suriname (Lynden 1939).
The Sipaliwini savanna ts part of a larger savanna complex
covering portions of Suriname and northern Para, Brazil
(Paru savanna). The current vegetation primarily consists
of grasses, sedges, scattered shrubs, trees, and Mauritia
palms (Oldenburger et al. 1973). The sharp demarcation
between the savanna and forest islands may be due to geo-
logical factors as suggested by Hoogmoed (1973), while
the anthropogenic influence of fires set during the dry sea-
son by the indigenous people might have been a reason
that the savanna remained open (Oldenburger et al. 1973;
Ouboter and Jairam 2012) [Fig. 1].
A number of factors potentially threaten the continued
existence of these populations of D. tinctorious in the wild.
Their extremely restricted range and small population
size are factors that increase the risk of extinction (Hall
et al. 2008). Anthropogenic fires could potentially reduce
December 2019 | Volume 13 | Number 2 | e210
The Blue Dyeing Poison-Dart Frog extant in Suriname based on a rapid survey
Fig. 1. Map of Suriname, South America (upper left inset) with approximate location of Sipaliwini savannah indicated by the black
box. Forest Islands are outlined in red and identified by numbers corresponding to those of Hoogmoed (1969, 2019). Arrows indicate
locations of the 50 x 50 m plots surveyed in Forest Islands 1, 2, and 4 during 16—18 June 2015. Forest Island 3 was not surveyed. In
this 2004 Google image, savanna vegetation surrounding the forest islands had been recently burned by indigenous hunters.
the size of the forest islands, and charred trees on the
periphery of the forest islands were noted by Cover (1997).
The emerging infectious disease Batrachochytrium
dendrobatidis (Bd) may put these populations at risk
(Courtois et al. 2012, 2015; James et al. 2015). Although
Bd has not been documented in Suriname, it has been
documented in D. tinctorius in French Guiana (Courtois et
al. 2015) which is east of Suriname. In addition, the blue
color morph of D. tinctorius occurring in the Sipaliwini
savanna is potentially vulnerable to rarity-fueled
exploitation for the pet trade (Hall et al. 2008).
Despite having been discovered almost 50 years ago
(Hoogmoed 1969), the only reported subsequent attempt
to ascertain the status of the blue morph of D. tinctorius in
the Sipaliwini savanna occurred in 1996 (Cover 1997). At
that time Cover (1997) found frogs but reported potential
evidence of illegal collection. Thus, the primary objective
of the current study was to determine the current status
(presence or absence) of D. tinctorius, in the Sipaliwini
savanna. If present, the plan was to establish survey plots
and conduct preliminary surveys to serve as benchmarks
for future population studies.
Materials and Methods
Survey plots. A survey plot measuring 50 x 50 m was
established in each of three forest islands which were
Amphib. Reptile Conserv.
separated by approximately 350-750 m of tall grass
savanna. Forest islands were identified using the same
numbering scheme as Hoogmoed (pers. comm.) [Fig.
1]. Survey plots within the forest islands measured
approximately 4% of 6 ha (Forest Island 1), 12.5% of
2 ha (Forest Island 2), and 6% of 4 ha (Forest Island
4) [Fig. 1]. Forest Island 3, which lies ~300 m north of
Forest Island 2, was not surveyed due to time constraints.
Plot placements were determined by entering each of the
forest islands and visually searching until a D. tinctorius
was encountered (Fig. 2). The nearest stream was then
used as one side of the 50 x 50 m sample plot, based
on previous research by Hoogmoed (1969) and Cover
(1997) citing stream preference by the frogs. Plot corners
were marked with GPS coordinates using a Garmin
60CSx. All three forest islands were subsequently
digitized using images from Google Earth Pro, which
were further edited in ArcMap, version 10.2, to show
the locations where the surveys were conducted. To do
this, Google Earth imagery was acquired and added as
a layer into ArcMap. Then Arc toolbox's KML layer
feature was used to transfer the digitized forest islands
created in Google Earth to ArcMap. The resulting image
emphasizes the presumed isolation by habitat of the D.
tinctorius populations from one another (Fig. 1).
Survey plots 1 and 4 were bordered on three sides by
small clear water streams. Survey plot 2 was characterized
December 2019 | Volume 13 | Number 2 | e210
d’Orgeix et al.
- 2: F ; :
Fig. 2. Dendrobates tinctorius from Sipaliwini savanna,
Suriname.
by having a small clear water stream at the lowest part
of the plot. Survey plot 1 was located on a north-facing
Slope that rose from 315-340 m in elevation. The area
was under a fully closed canopy forest with dense
understory vegetation interspersed with lianas. The forest
floor was covered by leaf litter, decomposing fallen
trees, and boulders of about 2—3 m in height and 3-6 m
in diameter (Fig. 3). Survey plot 2 was on a southeast
facing slope that rose from 315-325 m in elevation. The
plot was under a closed canopy with an open understory
and a forest floor covered by leaf litter. There were no
boulders in this plot. Survey plot 4 was on a west-facing
slope that rose from 300-350 m in elevation. The area
was under a fully closed canopy with dense understory
vegetation. One-third of the plot on the southwest side
had a dense understory of Phenacospermum sp. and
Poaceae bamboo species. The forest floor was covered
by leaf litter interspersed with 10-15 clumped boulders
that were about 1—3 m high and 1-5 m in diameter.
Survey methodology. Each plot was visually surveyed
once, for varying amounts of time, from 1030-1300 h.
Surveys occurred on 16—18 June 2015, three days after
the last rainfall on 13 June 2015. To survey a plot, nine
individuals were spaced approximately 1.5 m alongside
each other forming a line. Starting at one corner of the
plot, the surveyors walked 50 m to the opposite side of
the plot. Upon reaching the far side the surveyors again
spaced laterally starting 1.5 m from the person on the
farthest end to cover the next section, and walked back
towards the opposite side. This process was repeated until
the whole plot was surveyed. Survey participants wore
sterile disposable gloves which were changed between
the captures of each individual. Capture locations of
individual frogs were recorded as GPS coordinates using
a Garmin 60CSx. Frogs were then placed in individually
labeled Zip-Lock bags. Snout-vent length (SVL) was
measured to nearest 0.1 mm with digital calipers. Adults
were not sexed. After measurements were taken, each
frog was released at its original point of capture.
To identify potential changes in perimeter sizes of
the forest islands due to environmental or anthropogenic
Amphib. Reptile Conserv.
Fig. 3. Stream and boulder habitat in Survey Plot 1, Sipaliwini
savanna, Suriname.
factors, the most historical and most recent available
Google Earth images from 31 December 1969 and 17
November 2004 were used. These images were visually
compared by juxtaposing the forest islands outlined in
red, from 2004 (Fig. 4A) onto the 1969 image (Fig. 4B).
Statistical methods. A General linear model ANOVA
was used to compare SVL values between specimens
from each forest island. A f-test was used to compare
SVL of frogs measured in the current survey with those
reported by Hoogmoed (1969: Table I). SVL are reported
to nearest 0.1 mm + 1 SD. All analyses were conducted
using Minitab 17 statistical software (Minitab Inc., State
College, Pennsylvania, USA).
Results
Twenty-two adults and one juvenile were found in the
three forest island plots surveyed. Sixteen frogs were
found during the surveys, and seven were found adjacent
to the survey plots. Two frogs were found in Forest
Island 1 in 1 h (270 person-min/frog). Four frogs were
found adjacent to the survey plot in Forest Island 1 in
0.5 h (67.5 person-min/frog). Four frogs were found in
Forest Island 2 in 0.5 h (67.5 person-min/frog). Ten frogs
were found during the survey of Forest Island 4 in 1.5 h
(81 person-min/frog). Three frogs were found adjacent to
the survey plot in Forest Island 4 in 0.5 h (90 person-min/
frog). The overall mean yield of encounters was 115.2
person-min/frog. Variations in time spent conducting a
survey often reflected the difficulty in traversing the plot
based on the physical obstructions encountered (e.g.,
boulders and density of herbaceous undergrowth).
Adult SVL values ranged from 36.7-46.4 mm, with
a mean of 42.0 + 3.1 mm. No significant differences
between SVL of adult frogs from different forest islands
were found (one-way ANOVA: F,,,, = 0.23, P = 0.795).
No significant difference was found in a comparison
of SVL values recorded by Hoogmoed (1969) and the
current survey (t-test: t= 1.49, df= 44, P = 0.144). The
single juvenile recorded here measured 18.9 mm SVL.
A comparison of the vegetative perimeters of Forest
December 2019 | Volume 13 | Number 2 | e210
The Blue Dyeing Poison-Dart Frog extant in Suriname based on a rapid survey
ae rs
oa oie ae
\ he OE ee , 2 ae
eo te, a
Fig. 4. Forest Islands 1, 2, and 4, extant vegetation com
ze = kh
parison between Google Earth images for 2004 (A) and 1969 (B). Red
outlines delineating the three forest islands were juxtaposed from the 2004 image onto the 1969 image.
Islands 1, 2, and 4 appear almost identical in the two
Google Earth images taken in 2004 (Fig. 4A) and 1969
(Fig. 4B).
Discussion
Survey findings. The survey sites represented three of the
four forest islands where frogs were found in the surveys
by Hoogmoed (1969) and Cover (1997). In the current
surveys only adults were found, with the exception of
a single juvenile. No males transporting tadpoles were
found. Hoogmoed (1969) reported a male carrying two
tadpoles on his back on 30 September 1968, while Cover
(1997) who surveyed in June, did not note this behavior,
although he reported newly metamorphosed individuals
and tadpoles at two sites.
This survey recorded fewer frogs (23) than either
Hoogmoed (1969) or Cover (1997). Cover (1997, pers.
comm.) reported 56 frogs from Forest Island sites 1, 2,
and 4. Hoogmoed (1969, 2019) reported 82 frogs from
Forest Islands 1-4, during 11 different dates in 1968 and
1970. Differences in methodologies, season, and weather
limit most direct comparisons between these studies.
Both Cover (pers. comm.) and Hoogmoed (1969, 2019)
concentrated their searches in suitable habitat along
stream courses, while in the current survey the 50 x
50 m plots were centered around the spot where a frog
was first encountered. Weather events, such as rainfall,
presumably influence frog activity. For example, Cover
noted that after heavy rains at one site, the numbers of
frogs visible on the forest floor increased dramatically
(J. Cover, pers. comm.). A similar situation was also
reported by Wevers (2007). The current surveys took
place 3-5 days after the last rains. Hoogmoed (1969,
2019) reported 82 frogs during herpetological inventories
conducted on 11 different days in September and October
1968 and February 1970. In comparing the time required
to encounter a frog, Hoogmoed (2019) averaged 10.1
person-min/frog while the average in the current survey
was 115.2 person-min/frog. This would suggest a
Amphib. Reptile Conserv.
significant population decline if all other factors were
equal.
The blue morph of D. tinctorius in the Sipaliwini
savanna forest islands appears to be both geographically
and genetically isolated from other color morphs of D.
tinctorius 1n Suriname. The nearest known populations
of D. tinctorius, which are black and yellow dorsally, are
approximately 23 km north of the closest forest islands
surveyed (Fouquet et al. 2015). Blue morphs of D.
tinctorius in Sipaliwini are more than 300 km away from
the blue morphs reported by Silverstone (1975), and
approximately 315 km from the blue morphs reported by
Avila-Pires et al. (2010). In addition, the frogs in each of
the forest islands surveyed may be genetically isolated
from each other. Exploration of other remote forest
islands in the Sipaliwini savanna region may reveal
additional isolated populations of blue D. tinctorius.
Future molecular analyses could elucidate the genetic
divergence in these forest island populations since their
presumed isolation approximately 10,000 years ago
(Riezebos 1979).
Conservation considerations and future threats.
Batrachochytrium dendrobatidis (Bd) has been recorded
in French Guiana (Courtois et al. 2012, 2015) and Brazil
(Becker et al. 2016) which border Suriname to the east
and south, respectively. During this rapid survey no
dead frogs or frogs displaying visual symptoms of Bd
were found, although seemingly healthy specimens are
still known to be carriers of this disease (Coutinho et al.
2015).
While no evidence was found of illegal collecting for
the pet trade, that lack of evidence is not proof that it does
not occur or will not occur in the future. The indigenous
Trio peoples control both access to the transportation to
the savanna (canoes) and permission to visit the forest
islands where the frogs are found. Trio culture recognizes
the uniqueness of these frogs. Permission from the
village chief must be granted to visit the sites where frogs
may be observed, but collection 1s not allowed. This is
December 2019 | Volume 13 | Number 2 | e210
d’Orgeix et al.
enforced by the accompanying Trio guides. Presently,
the Trio people’s stewardship practices provide a large
measure of protection from collecting for the pet trade.
Sustainable programs that benefit the Trio community
should be implemented to reinforce their stewardship
of the habitat and wild populations of this unique color
morph.
Visual comparison of the perimeter size of these
forest islands between the 2004 and 1969 images do
not appear to indicate a significant change in size,
despite the history of anthropogenic fires (Fig. 4A,B).
Cover (1997) reported charred wood on the periphery
of the forest islands. However, when he observed a
fire in the savanna, it stopped when it reached the lush
vegetation on the perimeter of a forest island (J. Cover,
pers. comm.). Although the forest islands appear to be
stable in size, due to their small area and isolation, any
reduction in the water sources either through drought
or climate change could threaten both the forest island
vegetation and associated stream habitat. An increase in
xeric conditions could increase the risk of forest island
vegetation becoming drier on the periphery and thus more
susceptible to anthropogenic fires resulting in the edges
of these islands moving inwards, leading to a decrease in
their size or even complete destruction.
Barring direct human collection, climate change may
be the most serious threat to this unique blue morph of D.
tinctorius. There 1s a growing body of evidence that tropical
species will need to undergo elevational or latitudinal
range shifts to remain in analogous climatic conditions in
the future (Colwell et al. 2008; Nowakowski et al. 2016).
Given the isolated nature of these forest islands, their lack
of connectivity with either cooler forests or altitudinal
refugia, any change to the forest island habitat may be the
biggest threat to the continued survival of this unique D.
tinctorius blue morph in the wild.
Acknowledgements.—We would like to thank Paul
Ouboter from the National Zoological Collection of
Suriname for support and advice during the time spent
in Suriname. Dallas Davidson, Akira N. Harris, Ahnaia
White, Christian H. d’Orgeix, Sabria Greiner, and Alyssia
Velez participated in surveying the frogs. The Trio
people granted us permission to work in the Sipaliwini
savanna and provided lodging, transportation, and guides
to the sites. Marinus S. Hoogmoed and Jack Cover made
insightful comments to drafts of this manuscript, and
shared unpublished data and information. Tom Mathies
and Paul Kaseloo also provided helpful suggestions.
Permits for the fieldwork were granted by the Nature
Conservation Department of Suriname. This work was
supported in part by a grant to C. d’Orgeix through the
HBCU-UP of the National Science Foundation under
NSF Cooperative Agreement No. HRD-1036286. Any
opinions, findings, and conclusions or recommendations
expressed in this material are those of the author(s) and
do not necessarily reflect those of the National Science
Amphib. Reptile Conserv.
Foundation.
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Christian d’Orgeix is a behavioral ecologist and conservation biologist at Virginia State University.
Christian’s research focuses on the mating systems and conservation biology of reptiles and amphibians.
One of his current projects examines the probability of extinction of high- and low-elevation populations
of lizards. In Suriname, Christian and his students collaborate with Dr. Paul Ouboter and Rawien Jairam
from Anton de Kom Universiteit, Suriname, on studies on the behavior and conservation of frogs and
Rawien Jairam works at the National Zoological Collection of Suriname and is co-author of the book
Amphibians of Suriname. Rawien has an M.Sc. in Conservation Biology and has been interested in the
herpetofauna of Suriname for many years. Apart from general herpetology, he is specifically interested
in taxonomy and species distributions.
De'Jah T. Hardy is a junior Biology major at Virginia State University. De’Jah traveled to Suriname,
South America, to conduct research on frogs and ants. She also traveled to China to take Clinical
Medicine classes at Jinan University in Guangzhou. De’Jah’s goal is to explore as many opportunities as
she can as an undergraduate, and then go straight for her Master’s in Psychology. She plans to travel the
world someday, helping children as a traveling Occupational Therapist.
Sarah Melissa Witiak is a plant biologist who received her Ph.D. from Pennsylvania State University
(University Park, Pennsylvania, USA) and currently teaches at Virginia State University. Sarah is pri-
marily interested in the “pretty” parts of biology, including poison-arrow frogs, insect galls, and flower
evolution and ecology. Her current projects include studies of plant volatiles and a survey of insect gall
Laren Robinson worked as a GIS specialist at Virginia State University. She is currently pursuing
career options in GIS applications. (No photo available)
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e210
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 265-266 (e211).
Book Review
Night Lizards: Field Memoirs and a
Summary of the Xantusiidae
Howard O. Clark, Jr.
Colibri Ecological Consulting, LLC, 9493 North Fort Washington Road, Suite 108, Fresno, California 93730, USA
Keywords. Behavior, biogeography, ecology, reproduction, reptiles, Scincomorpha, Squamata
Citation: Clark HO Jr. 2019. Book review—Night Lizards: Field Memoirs and a Summary of the Xantusiidae. Amphibian & Reptile Conservation 13(2)
[General Section]: 265-266 (e211).
Copyright: © 2019 Clark. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 In-
ternational (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows:
official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 11 December 2019; Accepted: 11 December 2019; Published: 12 December 2019
Herpetologist Robert L. Bezy has produced a fascinating
memorr of his life and the lives of night lizards. When
reading about or researching night lizards, Bezy’s name
comes up often. When Bezy began his career there were
only a few night lizards known to science; now there are
35 living species in the family Xantustidae. The book
begins with a brief autobiography, detailing what mo-
tivated Bezy to pursue herpetology and what became a
long and winding road full of exciting discoveries and
working with some of the best herpetologists in the field.
Some of my favorite sections are where Bezy divides his
narrative into “locational highlights” and tells stories of
some experiences that had significant impacts on his life.
These stories are rich in landscape descriptions, wildlife
encounters, and how the adventure—planned or not—in-
fluenced the way he views life. These sorts of reflections
are priceless and allow the reader to reflect on his or her
own life. As I read through these stories I found myself
frequently reminiscing about my various encounters with
night lizards and other wildlife.
Following the autobiography and locational high-
lights, Bezy delves into the historical perspectives re-
garding night lizards. A “must read” is the account of
Janos Xantus and Spencer Fullerton Baird. Baird named
the night lizard genus (Yantusia) and family (Xantusi-
idae) after Xantus and interesting enough Xantus later
wrote to Baird that he didn’t even remember collecting
the small lizard. Other important perspectives include
those of John Van Denburgh, Edward H. Taylor, Hobart
M. Smith, Jay M. Savage, Robert G. Webb, Richard G.
Zweifel, and Charles H. Lowe. All of these men contrib-
uted to the natural history of the night lizards and Bezy
does a splendid job recapping their contributions.
Correspondence. howard.clark.jr@gmail.com
Amphib. Reptile Conserv.
NIGHT LIZARDS
Field Memoirs and a
Summary of the Xantusiidae
Robert L. Bezy
Title: Night Lizards: Field Memoirs and a Summary of the
Xantusiidae
Authors: Tell Hicks (Artist), Robert Bezy (Author)
Copyright: 2019
ISBN-10: 1938850599; ISBN-13: 978-1938850592
Publisher: ECO Herpetological Publishing
Pages: ii + 220; Price: USD $24.95
December 2019 | Volume 13 | Number 2 | e211
Night Lizards: Field Memoirs and a Summary of the Xantusiidae
Fig. 1. Nantusia aes nen the ear Desert, ieee Angeles
County, California. Photo by Howard O. Clark, Jr.
Another highlight of the book is the “questions” sec-
tion. Here, Bezy addresses a variety of natural history
aspects of the night lizard— undoubtedly questions that
he had over the years and now the reader has the oppor-
tunity to read the answers with Bezy as the messenger.
Topics include rock crevice ecology of the Xantusia and
Lepidophyma; night lizards in caves; island gigantism;
the species concept; the idea of unisexuals; night lizard
ecology; are night lizards nocturnal?; reproduction; so-
ciobiology; diet and predators; helminth parasites; ther-
mal and water ecology; movement, home range, and
population density; and conservation status.
The last half of the book provides a detailed discussion
about the night lizard family, Xantusiidae, followed by
the night lizard species accounts. Originally, the family
only had one species, Xantusia vigilis (Fig. 1), the small
lizard Janos Xantus collected at Fort Tejon, California.
But, eventually two other genera were added, Cricosaura
(Cuban night lizards), and Lepidophyma (tropical night
lizards). Bezy provides a detailed map that shows the dis-
tribution of the three genera and a diagram showing the
phylogenetic relationships. From there, each species has
its own detailed account, which generally includes these
sections: identification; chromosomes; size; distribution
and habitat; life history; sex ratio; etymology; conserva-
tion status; and discussion. Each account has a color pho-
to of the lizard, a colored distribution map, and photos
of representative habitat. With nearly 250 total figures
and photos throughout the book, the reader is treated to
a photo library that is unbeatable. Following the species
accounts is a night lizard species key—complete with
diagrams and photos. Also included are scale features for
differentiating night lizard species. The book ends with a
literature cited section which likely includes all the key
papers ever written on night lizards.
Overall, Bezy’s book is a must read for anyone inter-
ested in the story behind the night lizard, or in tales of
herpetological discovery and adventure in general. The
storytelling alone is reason enough to buy the book; the
photos, species accounts, range maps, etc., are a super
bonus and make the book the best resource currently on
this topic.
Howard O. Clark, Jr. has more than 20 years of professional wildlife and research experience. Howard
is certified by the Ecological Society of America as an ecologist and by The Wildlife Society (TWS) as a
Certified Wildlife Biologist®. His work as an ecological consultant has focused on the fauna and ecosystems
of California and has included extensive baseline inventories, surveys for rare animals, and habitat
assessments. He has conducted dozens of inventories, surveys, and assessments for Blunt-nosed Leopard
Lizard, Western Burrowing Owl, San Joaquin Kit Fox, Giant Kangaroo Rat, and Mohave Ground Squirrel
among many others. Howard developed his consulting skills while working for H. T. Harvey & Associates
(Los Gatos, California) for 10 years and Garcia and Associates (Auburn, California) for three years. He
currently works for Colibri Ecological Consulting, LLC, as a Senior Scientist in Fresno, California. Prior
to working as a consultant, Howard spent seven years as a wildlife biologist with the Endangered Species
Recovery Program (California State University, Stanislaus Foundation, Turlock, California). He completed
his Master’s degree at CSU, Fresno in 2001. His thesis addressed the interactions between the endangered
San Joaquin Kit Fox and the non-native Red Fox in Kern County, California. Howard is an instructor for
TWS kit fox and small mammal workshops, and the Western Section of TWS awarded him the Raymond
F. Dasmann Award for Professional of the Year in 2015. He is the Layout Editor for the Western Section’s
journal, Western Wildlife, as well as three herpetological journals: Amphibian & Reptile Conservation,
Sonoran Herpetologist, and Herpetological Conservation and Biology. During leisure time, Howard enjoys
hiking, geocaching, and visiting places of historical interest with his daughter.
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e211
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 267-275 (e212).
Impacts of a highway on the population genetic structure of a
threatened freshwater turtle (G/lyptemys insculpta)
12.*Alexander J. Robillard, ?Sean Robinson, 7Elizabeth Bastiaans, and 7Donna Vogler
'Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, Maryland, USA *Department of Biology,
State University of New York College at Oneonta, Oneonta, New York, USA
Abstract.—Genetic partitions for members of the family Emydidae often correspond with both natural and
anthropogenic landforms. For semi-terrestrial turtles, clear negative impacts are associated with habitat
fragmentation via roadways, such as loss of breeding individuals, increased inbreeding, and decreased migration.
The Wood Turtle (Glyptemys insculpta) is a Species of Special Concern in New York and native to the central
portion of the state, where Interstate Highway 88 was constructed in the 1970s. To examine possible impacts of
the highway on local populations, a museum collection of Wood Turtles that predates road construction was used.
Specifically, microsatellite markers were used to compare historic (n = 38) and contemporary (n = 26) Wood Turtle
DNA from opposite sides of the highway. The measured parameters were inbreeding (F,.), differentiation (F.,),
number of breeding individuals (N.), migration (m), and overall population genetic structure. The populations on
either side of the highway were predicted to have become more differentiated and inbred over time, and migration
was predicted to decrease over time. Overall, populations on either side of the interstate were historically a single
population, had a greater number of breeding individuals, and were less differentiated. No change in inbreeding
was found across time. These findings suggest there is more migration, running north to south between the two
populations, likely attributable to the directionality of the flow associated with local creeks. Further research
examining these two separate populations within the context of the entire state is necessary to determine whether
they should be treated as separate Conservation Units.
Keywords. Emydidae, habitat fragmentation, roadways, microsatellite, population structure
Citation: Robillard AJ, Robinson S, Bastiaans E, Vogler D. 2019. Impacts of a highway on the population genetic structure of a threatened freshwater
turtle (Glyptemys insculpta). Amphibian & Reptile Conservation 13(2) [General Section]: 267-275 (e212).
Copyright: © 2019 Robillard et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 22 February 2018; Accepted: 24 April 2019; Published: 23 December 2019
Introduction al. 2000). In North America, several case studies have
suggested that anthropogenic disturbances, particularly
On a global scale, amphibians and reptiles are in
decline due to pressures which include climate
change, unsustainable harvest, habitat loss, and habitat
degradation (Gibbons et al. 2000). Among all reptile and
amphibian species, members of the order Testudines are
particularly vulnerable to increased decline when faced
with increasing anthropogenic disturbances, such as road
mortality and illegal harvesting (Lieberman 1994; Garber
and Burger 1995; Wood and Herlands 1997; Williams
1999: Levell 2000; Gibbons et al. 2000; Gibbs and
Shriver 2002; Steen and Gibbs 2004; Gibbs and Steen
2005; Steen et al. 2006; USFWS 2015). Nearly half of
all turtle species are currently categorized as threatened
or endangered (Rhodin et al. 2011). Terrestrial turtles
are generally perceived as poor long-distance dispersers.
Limitations to dispersal enable habitat fragmentation,
which can put populations at risk of extinction due to
demographic and genetic diversity loss (Gibbons et
Correspondence. “ajrobill@umd.edu
Amphib. Reptile Conserv.
roadways, have direct negative impacts on freshwater
turtles by skewing sex ratios and increasing the mortality
of migrating individuals (Buhlman and Gibbons 1997;
Wood and Herlands 1997; Williams 1999; Levell 2000;
Gibbons et al. 2000; Gibbs and Shriver 2002; Steen and
Gibbs 2004; Gibbs and Steen 2005; Steen et al. 2006;
USFWS 2015).
When assessing the negative impacts of fragmented
populations, genetic markers can identify dispersal
pathways and population diversity (Lamb et al. 1989;
Galbraith et al. 1995). For example, studies focusing
on turtle populations have found river drainages and
intermontane basins to be barriers to gene flow (Gibbs
and Amato 2000). Similarly, several studies have
identified relatively high allelic diversity in Wood
Turtle populations when compared to other species
(Gibbs 1993; Tessier et al. 2005; Amato et al. 2008;
Castellano et al. 2009; Spradling et al. 2010). Given
December 2019 | Volume 13 | Number 2 | e212
Population genetics of Glyptemys insculpta in New York
Otsego (North) an d Delaware (South)
Counthes bisected by Interstate £3 and
the Susquehanna River
Fig. 1. Study area. Interstate Highway 88 (I-88) and the Susquehanna River (Susq.) bisect Otsego and Delaware Counties, New
York, USA.
their poor long-distance dispersal ability, populations of
freshwater turtles could be at increased risk from habitat
fragmentation via natural or anthropogenic barriers,
which may result in loss of genetic and demographic
connectivity (Gibbons et al. 2000; Gibbs and Amato
2000). Specifically, turtles which do attempt to move
long distances within a fragmented landscape, as females
often do for nesting, may be at greater risk of dispersal
related mortality, e.g., roadkill (Gibbs and Shriver 2002:
Steen and Gibbs 2004). Road mortality driven by habitat
fragmentation is believed to be the culprit for the gradual
skewing of sex ratios and the general decline of female
turtles among many freshwater turtle species throughout
the United States (Steen and Gibbs 2004; Gibbs and
Steen 2005; Steen et al. 2006).
Known to disperse both long and short distances
(Harding and Bloomer 1979) throughout its range, the
Wood Turtle (G/yptemys insculpta) is a Species of Special
Concern in New York State, which may be at risk from
the demographic and genetic impediments associated
with habitat fragmentation (Gibbons et al. 2000; Breisch
and Behler 2002; Tuttle and Carroll 2003; Arvisais et al.
2004; Sweeten 2008). Limitations to dispersal within
fragmented landscapes are believed to contribute to
the decline of wetland-dependent turtles (Gibbs 1993;
Tessier et al. 2005; Amato et al. 2008; Castellano et al.
2009; Spradling et al. 2010). Although previous studies
have examined Wood Turtle population genetics, none
have focused on the potential impacts that anthropogenic
Amphib. Reptile Conserv.
habitat fragmentation could have on regional populations
(Tessier et al. 2005; Amato et al. 2008; Castellano et al.
2009; Spradling et al. 2010).
Between 1974 and 1980, Interstate Highway 88 (I-
88, 193 km) was built across eight Central New York
counties (Fig. 1), including Otsego and Delaware
counties (Associated Press 1986; Edwardsen 1989).
Prior to this, from 1958-1968, Dr. John New collected
and dry-preserved Wood Turtles (n = 300) from across
New York state, including sites north and south of
I-88. Using this historic data set in conjunction with
contemporary data, this study examines the potential
impacts of building a large interstate highway on a
vulnerable turtle species over a 60-year period. Over
that same 60-year period, New York State has become
more populated, according to U.S Bureau of Census
data for 1960-2010. Given that wetland habitat size
and connectivity degrade with increased human activity
(Gibbs 2000), and that such disruption of wetland
mosaics can have dramatic negative impacts on semi-
terrestrial turtle populations (Gibbs and Shriver 2002),
declines are expected to be observable on the genetic
scale. Specifically, an increase in genetic differentiation
between populations (F,,), a decrease in the effective
breeding population size (N,) between sampling sites
on either side of Interstate 88, and limited gene flow
between populations on either side of the highway are
expected. Here, microsatellite data are used to examine
these critical genetic parameters.
December 2019 | Volume 13 | Number 2 | e212
Robillard et al.
Materials and Methods
Study sites: Contemporary (n = 26) and historic (n
= 38) data were collected from two streams in Otsego
County and two streams in Delaware County, New York.
The furthest sections of the two Otsego County streams
sampled are rectilinearly 11 km and 28 km north of
Interstate 88. The furthest sections of the two Delaware
county streams sampled are rectilinearly 3 km and 9 km
south of Interstate 88. All streams sampled are part of the
Susquehanna watershed, and terminate on the southern
side of Interstate 88 (Fig. 1). Contemporary sites were
sampled during the spring/early summer and late fall
active periods of 2015 and 2016 using the Regional
Conservation Needs protocol, which involves sampling
in 1 mi increments (Jones et al. 2015).
Samples: Blood samples were used for contemporary
data, and | mm tail tips were harvested from dried
historic specimens. Blood samples (0.1—0.5 ml) were
collected from the dorsal coccygeal vein using a sterile
1.0 ml 25-gauge syringe (Jones et al. 2015). Blood
was transferred into test tubes immediately upon
return from the field and stored in 1:1 1 x PBS buffer
in a -20 °C freezer. Genomic DNA was extracted from
each sample using the QIAGEN DNeasy Blood and
Tissue Kit (Qiagen, Inc., Valencia, California, USA).
Tail tips were digested in Proteinase K for 36 h. Each
extracted sample was stored in a -20 °C freezer. Seven
microsatellite loci were examined (GmuD16 [Genbank
accession number: AF516235], GmuD40 [AF517244],
GmuD51 [AF517239], GmuD87 [AF517244], GmuD88
[AF517245], GmuD93 [AF517248], and GmuD95
[AF517249]) using primers initially designed for a close
relative of the Wood Turtle, Glyptemys muhlenbergii
(King and Julian 2004). Samples were amplified
using the QIAGEN Multiplex PCR kit (Qiagen, Inc.,
Valencia, California, USA) and a modified version of
the PCR protocol (Castellano et al. 2009). The length
of the extension step from this protocol was doubled to
optimize historic sample amplification due to the highly-
fragmented nature of this DNA. PCR products were
analyzed at the Cornell Biotech Institute in Ithaca, New
York, and visualized using GENEMARKER version
2.6.7 (Hulce et al. 2011).
Statistical analysis: MICROCHECKER version 2.2.3
was used to test each locus for the presence of null alleles,
scoring errors, and large allele dropout (Van Oosterhout
et al. 2004). Clustering was used to assign individuals
to populations using the program STRUCTURE version
2.2 (Pritchard et al. 2000; Falush et al. 2003). Data
were analyzed for all contemporary and historic turtles
from each of the sites north (Otsego County) and south
(Delaware County) of Interstate 88. For each analysis,
three runs were used for each value of K (number of
assumed populations) ranging between one and nine.
Amphib. Reptile Conserv.
A 106 burn-in period was used, and 106 Markov Chain
Monte Carlo (MCMC) iterations were used in the default
“admixture model” of ancestry and correlated allele
frequencies. Population origin data (north and south)
were provided for each individual. Mean log likelihood
and DK values were used to assign individuals to
populations [K] (Evanno et al. 2005).
Deviations from the Hardy-Weinberg (HWE)
expectation among pairs of loci were tested along
with mean heterozygosity, allelic richness, numbers
of private alleles, inbreeding coefficient (F,.), genetic
differentiation (F..), and effective population size (N,)
using GenAIEx version 6.5 (Peakall and Smouse 2006,
2012) for the populations north (Otsego) and south
(Delaware) of Interstate 88. The comparison of historic
and contemporary loci F,. was made using a student’s
t-test. Evidence of a bottleneck on the contemporary
data was tested using the program BOTTLENECK
(version 1.2.02, Cornuet and Luikart 1996) with an
infinite allele model (IAM) and the two-phase model
(TPM) recommended by Luikart et al. (1998) over
10,000 iterations. The significance of Wilcoxon test
score output (a = 0.05) and mode shift were both used
as evidence of a bottleneck (Cornuet and Luikart 1996;
Luikart et al. 1998; Chiucchi and Gibbs 2010). Short-
term migration (m) between the “last few generations”
was estimated using Bayesian inference software
BAYESASS (version 3.03, Wilson and Rannala
2003) using 3 x 107 iterations with two long-chains
sampling every 2,000 iterations, and this included
a burn-in of 107. Specifically, a time span reaching
back < 5 generations, or 25-125 years (Chuicchi and
Gibbs 2010) was used since the estimated generation
time for Wood Turtles 1s 25 years (Farrell and Graham
1991; Galois and Bonin 1999). Multiple independent
model runs were made using a random seed, with final
selection made based on Maximum Likelihood (e.g.,
Chuicchi and Gibbs 2010).
Results
Six of the seven microsatellites amplified consistently.
The exception was GmuD51, which was removed
from further analyses. Historic specimens had a high
allele dropout rate (46%), which is expected for highly
fragmented antique DNA (Mills et al. 2000; Sefc et
al. 2003). No evidence of genotyping error or null
alleles was found for those that amplified. Sample size,
effective population size, heterozygosity, and overall
differentiation between north and south populations, for
both historic and contemporary data, are summarized
in Table 1. F,, values for the contemporary populations
was 0.166, while historically they were estimated at
0.081 (Table 2). Heterozygosity estimates per locus are
summarized in Table 2. Northern contemporary and
historic data each showed three of six loci out of HWE.
Southern contemporary data displayed four of six loci
December 2019 | Volume 13 | Number 2 | e212
Population genetics of Glyptemys insculpta in New York
North
0.869
(SD: 0.054)
Confidence Interval
(0.761 - 0.969)
a=I11
——-
m = 0.044 (SD: 0.040)
Confidence Interval
(0001 - 0.150)
ai = 0.241 (SD: 0.037)
Confideoce Interval
(0.166 - 0.302)
aaa
South
0.707
(SD: 0.034)
Confidence Interval
(0.668 - 0.786)
n= 15
Fig. 2. Estimate of short-term gene flow among populations
north and south of Interstate Highway 88 (gray bar) and the
Susquehanna River (dashed line) shown with 95% confidence
intervals. Circle size reflects relative sample size. Values inside
of circles represent the contribution of gene flow from within
populations.
out of HWE, while the southern historic data displayed
a single locus out of HWE. Comparison of historic and
contemporary inbreeding (F,.) indicated no difference
between estimations (P = 0.30). Fixation indexes for
each locus are summarized in Table 3.
Contemporary samples clustered into two populations
(K = 2, Ln P(D) = -659.5, Var [LnP(D)] = 74.5), with
a clear distinction between north and south samples.
Historic samples consistently clustered into a single
population (K = 1, LnP(D) = -787.9, Var [LnP(D)]
= 33.0). There was a deficiency of heterozygosity (P
0.04) for the northern contemporary population
under the Wilcoxon rank sign test in the TPM model.
Specifically, none of the northern loci were in mutation-
drift equilibrium, as five of six loci showed signs
of heterozygosity deficiency with the final locus in
excess under the IAM model. Southern contemporary
populations showed no sign of a genetic bottleneck.
Short-term migration (m) was conservatively estimated
to be higher going from north to south (24%) than south
to north (4.4%) [Fig. 2].
Discussion
Genetic changes and trends in turtle populations may be
difficult to detect due to their naturally long generation
times and long lives (Gibbs and Amato 2000). Using
the genetic material available from historic samples
allowed the successful detection of changes between
the populations across a relatively brief period of
time. Although this study used a limited number of
microsatellites (six of seven), the polymorphic nature
of the markers and highly differentiated level of the
populations suggest that the results capture an adequate
amount of information for comparative genetic analysis
(Kalinowski 2002, 2005; Arthofer et al. 2018), especially
given the sample sizes for the historic and contemporary
populations (Hale et al. 2012). Specifically, the results
indicated that these local populations have likely become
genetically fragmented over the last 60 years. This may
indicate that certain freshwater turtle populations are
more vulnerable, in terms of the rate of change, to shifts
in genetic structure than previously thought.
Structural analysis of the contemporary data revealed
that Wood Turtle populations clustered into two
populations, where historically, they were likely a single
interconnected unit. In addition, the same samples revealed
that local populations have become more differentiated
over time as an increase of F , was observed from 0.081
in historical to 0.166 in contemporary populations. This
shift from moderate differentiation (> 0.05) to great
differentiation (> 0.1) over an evolutionarily short period
of time would appear to be aberrant when compared to
previous studies examining Wood Turtle differentiation
(Hartl and Clark 1997). However, Tessier et al. (2005)
sampled Wood Turtles in a similar semi-montane habitat,
and found that some of their populations, which had a
proximity between sites comparable to those in the
current study (~15—50 km), had similar differentiation
as the historic samples studied here. Conversely, the
contemporary sample differentiation found here is more
similar to that of their sites which were much further apart
Table 1. Summarized outputs of population parameters from GenAIEx v 6.5. Parameters displayed are sample size (n), effective
population size (N.), observed (H,) and expected (H,) heterozygosity, and overall differentiation (F,,) between North and South
collecting sites.
Historic (1955-1965)
n N, (SE) Mean # alleles (SE)
North 20 6.9 (1.5) 10.0 (1.5)
South 18 513°C.) 7.8 (1.6)
Total 38 122
Contemporary (2015-2016)
North 11 4.0 (0.4) 6.3 (0.5)
South 15 7.0 (0.8) 11.0 (0.8)
Total 26
Amphib. Reptile Conserv. 270
H, (SE) H, (SE) Private alleles soe
0.61 (0.11) 0.82 (0.04) 40
0.65 (0.14) 0.77 (0.04) 27 0.081
0.67 (0.04) 0.74 (0.02) 12
0.81 (0.04) 0.85 (0.02) 19 0.166
December 2019 | Volume 13 | Number 2 | e212
Robillard et al.
Table 2. Summarized contemporary observed (H,) and expected (H,) heterozygosity.
Locus Size range (bp) # of alleles
GmuD16 165-296 24
GmuD87 238-394 24
GmuD88 114-264 30
GmuD93 125-389 20
GmuD95 122-266 24
GmuD40 157-280 21
(> 60 km) than the sites in this analysis (Tessier et al.
2005). Overall, this suggests the populations examined
here, which are relatively close to one another in terms
of physical distance, possess genetic differentiation
that is more akin to areas further apart, implying that
there is a barrier preventing genetic exchange between
them. In flatter areas along the coastal plains of the
northeastern United States, differentiation among Wood
Turtle populations is essentially non-existent, enabling
populations to be panmictic across separation distances
greater than 40 km (Castellano et al. 2009). This leads
us to believe that dispersal limitation is due to some
environmental factor, and not simply life history.
A study on another terrestrial emydid turtle, Jerrapene
ornata (Ornate Box Turtle), in Texas found that a major
highway built in 1937 was likely the cause of significant
differentiation between populations on either side, but not
the cause of a change in overall structure (Richtsmeier
et al. 2008; Cureton et al. 2014). Similarly, Tessier et
al. (2005) found that the St. Lawrence River acts as a
barrier between Wood Turtles on either side of its shores,
separating them structurally. It is possible that the
observed structural separation between the populations
studied here has been compounded by the combination
of the intertwining bisection of Interstate 88, and the
Susquehanna River (Fig. 1).
Despite the findings of Tessier et al. (2005), the
migration analysis output in this study (Fig. 2) may
suggest that flooding events are allowing at least
some unidirectional gene flow to persist between the
populations on either side of Interstate 88. In short, local
hydrology from lower order streams at both the north
North South
H, H, H, H,
0.700 0.830 0.857 0.829
0.700 0.840 0.857 0.768
0.733 0.849 0.867 0.838
0.333 0.736 0.714 0.885
0.778 0.833 0.667 0.871
0.778 0.747 0.917 0.892
and south sampling sites terminate at the Susquehanna
River south of Interstate 88. Research by Jones and
Sievert (2009) indicates that flooding events, which have
dramatic impacts on Wood Turtles, may play a vital role
in connectivity. Specifically, flood events can displace a
substantial (40%) portion of Wood Turtle subpopulations
by long distances (1.4—-16.8 km) downstream (Jones and
Sievert 2009), which may explain the unidirectionality of
the migration estimates found here (Fig. 2).
This possibility seems even more likely when
considering the local footprint of Interstate 88, much of
which is built on steep and sometimes craggy mounds
protruding from the stream and forest surface. These
mounds, which span four total lanes and occasionally
split with a center depression or open fall at the median
strip, most likely make terrestrial genetic exchange near
impossible between the north and south populations.
Moreover, the Susquehanna in its entirety is substantially
narrower than the St. Lawrence River (Kammerer 2005),
which may make survival of flooding events more
likely. Additionally, we observed Wood Turtles using the
Susquehanna’s embankments and flood plains with some
regularity, so although its flow may prevent and influence
movement, it should not be considered an insurmountable
genetic barrier like the much larger St. Lawrence (Tessier
et al. 2005). As such, it is likely that Wood Turtle
movement is influenced by the directionality of the flow
in creeks and rivers, and may explain the unidirectional
migration observed here (Fig. 2).
Although some streams and creeks in Delaware
County run north to south as they percolate down from
the Catskill mountains, the northern Delaware drainages
Table 3. Microsatellite fixation indexes for both historic and contemporary populations.
Historic
Locus K ",
GmU16 0.245 0.308
GmU87 -0.246 -0.045
GmU88 0.253 0.282
GmU93 0.956 0.961
GmU95 0.136 0.171
GmU40 -0.028 0.024
Mean 0.220 0.284
SE 0.166 0.147
Amphib. Reptile Conserv.
Contemporary
st F, it st
0.084 0.093 0.226 0.146
0.161 -0.056 0.102 0.150
0.038 0.030 0.157 0.131
0.110 0.117 0.367 0.283
0.040 0.166 0.270 0.125
0.051 -0.048 0.117 0.158
0.081 0.050 0.206 0.166
0.020 0.037 0.041 0.024
271 December 2019 | Volume 13 | Number 2 | e212
Population genetics of Glyptemys insculpta in New York
near the sampling sites used in this study flow south
to north, terminating into the Susquehanna. Previous
research by Brown et al. (2016) indicated that Wood
Turtles become more terrestrial as the thermoregulatory
benefits of returning to the water at night diminish
during the summer, but they never seem to stray too
far from flowing water. Furthermore, a species of turtle
that divides its time between land and water (Kaufmann
1992) is expected to use smaller rivers as corridors like
many other turtle species (Gibbs and Amato 2000). If
local Wood Turtles are using the Susquehanna River as
a corridor at least in part, with strong flow and flooding
events acting as a migration regulator, further genetic
research should yield an F., gradient and not complete
differentiation. In other words, central New York’s
populations should be progressively more differentiated
from populations further south along the Susquehanna
River, but not completely differentiated altogether.
Therefore, further research should investigate the
potential of large rivers, namely the Susquehanna River,
to act as turtle barriers or corridors.
If the Susquehanna is acting as a unidirectional
barrier, long-term declines could prove problematic for
the local populations. Specifically, the loss of only a few
individuals may appear to be minimal in terms of allelic
diversity, but a negative change in the effective breeding
population (N,), as was observed, could prove to have
adverse conservation consequences. For example, similar
rates of reduction in Bog Turtle populations have been
identified as substantially increasing the likelihood of
extirpation (Shoemaker 2011). Certain life histories are
also known to be susceptible to such impacts (Jonsson and
Ebenman 2001). Specifically, for Bog Turtle populations,
the loss of only a few breeding adult individuals can have
greater impacts on populations than even dramatic short-
term increases in juvenile mortality (Shoemaker 2011).
Similar losses for Wood Turtles, the closest known
relative of the Bog Turtle, could prove to be equally
problematic. This vulnerability, again, would be due to
their long generation times, high juvenile mortality rate,
and reliance on adult survival to bolster the populations
(Gibbs and Amato 2000). This situation presents a suite
of unique conservation issues which are likely to also be
applicable to other freshwater turtle species.
One noteworthy observation here is that the bottleneck
analysis presented identified both heterozygosity
deficiency and excess in the northern populations.
Typically, heterozygosity deficiency is associated with
a founder effect (Cornuet and Luikart 1996) or possibly
the existence of a subpopulation structure within the
sample, known as the Wahlund effect (Wahlund 1928).
However, in rare situations when allelic diversity is high,
as itis with the Wood Turtles in this study, heterozygosity
deficiency can be the result of post-bottleneck changes,
such as mutation or population expansion, which fill the
allelic gaps left by limited random selection (Cornuet and
Amphib. Reptile Conserv.
Luikart 1996; Maruyama and Fuerst 1985). For freshwater
turtle populations, which typically have a small number
of long-lived adults possessing the majority of effective
alleles (Crouse and Frazer 1995; Gibbs and Amato 2000),
the loss and sequential replacement of these few valuable
reproductive individuals appear to enable this particular
scenario. Considering that none of the loci for the
northern population were in mutation-drift equilibrium,
and they showed evidence of deficiency and excess, it
seems clear that something has impacted the northern
population allelic ratios. Further research into Otsego
County’s populations north of Interstate 88 is required
to determine the source of this irregularity. Additionally,
we recommend that future management plans for Wood
Turtle populations in central New York and other regions
with montane-riverine mosaics consider the potential
genetic complications associated with anthropogenic
habitat fragmentation. To mitigate these potential
impacts, the installation of appropriately sized culverts,
drift nets, and turtle-crossing signs (Aresco 2005; Woltz
et al. 2008), in high-density areas (Gunson and Schueler
2012), is necessary.
Conclusions
Consistent with other research (Steen and Gibbs 2004;
Gibbs and Steen 2005; Steen et al. 2006) the observed
division and reduction in N, in the local populations
studied here, the potential recent genetic bottleneck,
the increased differentiation, and the overall change in
population structure are most likely attributable to the
additional fragmentation of the local montane/riverine
habitat by the bisecting interstate highway. A clear
north to south directionality of gene flow was observed
from the short-term (25—125 years) migration estimate.
The full implications of this dichotomy, in the context
of potential isolation due to fragmentation, have yet to
be determined. As a species of conservation concern,
understanding the genetic landscape at the local and
regional levels is vital for planning future management.
In terms of conservation, it is possible New York’s central
populations hold unique alleles as they are surrounded by
three major highways and two large mountain ranges. In
turn, this may require that management efforts treat these
isolated populations as demographically independent
units, should they yield unique genetic variation. As
such, we recommend that policy and management
reflect the impacts that bisecting highways can have
on populations within a local region, and not just those
adjacent to a thoroughfare. Additionally, we recommend
that policy and management efforts reflect the evidence,
which suggests that hydrology may dictate Wood Turtle
gene flow. Furthermore, research focused on determining
where central New York’s populations fit within the
context of the entire region’s genetic landscape will be
particularly useful.
December 2019 | Volume 13 | Number 2 | e212
Robillard et al.
Acknowledgments.—This research was funded by
the State University of New York College at Oneonta
Sponsored Programs research grant, the Western New
York Herpetological Society’s Marv Aures and Bob
Krantz research grant, the Huyck Preserve research grant,
and the State Wildlife Grant (SWG) Program. Special
thanks to E. Clifton, S. Fontaine, W. O’Connell, and S.R.
Talley for providing field and lab assistance. Wood Turtle
handling and tissue collection was permitted by the New
York State Department of Environmental Conservation
(NYSDEC; Science Permit #139) and was approved by
the SUNY-Oneonta Institutional Animal Care and Use
Committee. We are appreciative of the initiated fieldwork
and consultation of Dr. Tom Akre, Dr. Glenn Johnson,
Dr. Mike Jones, Dr. Angelena Ross, Bill Hoffman, and
Michael Musnick.
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Alex Robillard received a B.S. in Conservation Biology from State University of New York, College of
Environmental Science and Forestry (SUNY-ESF, Syracuse, New York, USA), and an MLS. in Biology
from SUNY-Oneonta. Currently a predoctoral fellow at the Smithsonian Data Science Lab and National
Zoo, and a Ph.D. student in the Marine-Estuarine and Environmental Science Program at the University
of Maryland, Alex’s dissertation focus is on the conservation and population genetics of the Eastern
Pacific Hawksbill Sea Turtle. His past research had focused on the ecology of the Bog Turtle, Wood
Turtle, and Eastern Massasauga Rattlesnake in New York State. Alex is also researching how deep
machine learning and computer vision can be used to combat the poaching of sea turtles.
Sean Robinson completed a B.A. at Hartwick College (Oneonta, New York, USA), an M.S. at SUNY-
ESF, and a Ph.D. at the University at Albany, New York. Dr. Robinson joined the SUN Y-Oneonta
faculty in 2010 where his research is focused on understanding how the mode of reproduction in plants,
particularly bryophytes, affects colonization of new habitats, range expansions, and the exchange of
alleles both within and between populations. Additionally, Dr. Robinson conducts research focused on
vegetation dynamics on alpine summits, using molecular techniques to identify population structuring.
Elizabeth Bastiaans completed a B.A. at the University of Chicago, a Ph.D. at the University of
California, Santa Cruz, and a postdoctoral fellowship at the University of Minnesota, Twin Cities.
Elizabeth joined the SUNY-Oneonta faculty in 2015. Her previous research focused on sexual signal
evolution in Mexican montane lizards and life history evolution in tropical crickets. At SUN Y-Oneonta,
Dr. Bastiaans has started to focus her research on the reproduction and physiology of the Wood Turtle
across New York State, while maintaining her previous collaborations with colleagues in Mexico.
Donna Vogler was born and educated in the Midwestern United States, with a B.S. from The Ohio
State University, and an M.S. from Iowa State University, before working for the U.S. Fish and Wildlife
Service in Washington, DC. Donna earned a Ph.D. from Penn State University in Botany, and was a post-
doctoral researcher at the University of Pittsburgh before joining the SUNY-Oneonta faculty in 2000. Dr.
Vogler’s recent research topics include demographic studies of invasive plant species (e.g., Marsh Thistle,
Cirsium palustre), floral mechanisms related to self vs. outcross pollination, and using Wood Turtle habitat
communities and vegetation management at regional airports to reduce wildlife hazards.
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e212
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 276-298 (e213).
Modelling the distribution of the Ocellated Lizard in France:
implications for conservation
1*Pierre Jorcin, 7Laurent Barthe, *Matthieu Berroneau, ‘Florian Dore, °Philippe Geniez, °Pierre
Grillet, “Benjamin Kabouche, *Alexandre Movia, °Babak Naimi, ‘°Gilles Pottier, ‘Jean-Marc Thirion,
and ‘*Marc Cheylan
'Naturalia-Environnement, Site Agroparc, rue Lawrence Durrell, 84911 Avignon, FRANCE *!°Nature En Occitanie, Maison régionale de
l’Environnement, 14 rue de Tivoli, 31000 Toulouse, FRANCE ?Cistude-Nature, Chemin du Moulinat, 33185 Le Haillan, FRANCE +3 Chemin de
Saint-Jacques, Faugerit, 79120, Chey, FRANCE »*'*Laboratoire Biogéographie et Ecologie des Vertébrés — CNRS, PSL Research University, EPHE,
UM, SupAgro, IRD, INRA, UMR 5175 CEFE, 1919 route de Mende, Montpellier, FRANCE °10 rue de la Sayette, 79340 Vasles, FRANCE ‘Ligue
pour la Protection des Oiseaux Provence-Alpes-Cote d’Azur (LPO PACA), 6 avenue Jean Jaurés, 83400 Hyéres, FRANCE *Ligue pour la Protection
des Oiseaux Dréme (LPO Droéme), 18 place Génissieu, 26120 Chabreuil, FRANCE °Department of Geosciences and Geography, University of
Helsinki, 00014, PO Box 64, Helsinki, FINLAND ''Objectifs Biodiversité, 22 rue du Dr. Gilbert, 17250 Pont-l’Abbé-d’Arnoult, FRANCE
Abstract—The Ocellated Lizard, Timon lepidus (Daudin 1802) occupies the Mediterranean regions of
southwestern Europe (Portugal, Spain, France, and the extreme northwest of Italy). Over the last decades, a
marked decline in its population has been observed, particularly on the northern edge of its distribution. As a
result, it is currently considered a threatened species, especially in France and Italy. In France, a national action
plan for its conservation has been put in place. In this study, ecological niche modelling (ENM) was carried out
over the entire area of France in order to evaluate the species’ potential distribution, more accurately define its
ecological niche, guide future surveys, and inform land use planning so this species can be better taken into
consideration. The modelling used data representing 2,757 observation points spread over the known range
of the species, and 34 ecogeographical variables (climate, topography, and vegetation cover) were evaluated.
After removing correlated variables, models were fitted with several combinations of variables using eight
species distribution model (SDM) algorithms, and then their performance was assessed using three model
accuracy metrics. Iterative trials changing the input variables were used to obtain the best model. The optimized
model included nine determining variables. The results indicate the presence of this species is linked primarily
to three climate variables: precipitation in the driest month, precipitation seasonality, and mean temperature
in the driest quarter. The model was checked by a sample dataset that was not used to fit the model, and this
validation dataset represented 25% of the overall field observations. Of the known occurrence locations kept
aside to check the results, 94% fell within the presence area predicted by the modelled map with a presence
probability greater than 0.7, and 90% fell within the area with a presence probability ranging from 0.8 to 1, which
represents a very high predictive value. These results indicate that the models closely matched the observed
distribution, suggesting a low impact of either geographical factors (barriers to dispersal), historical factors
(dispersal process), or ecological factors (e.g., competition, trophic resources). The overlap between the
predicted distribution and protected areas for this species reveals that less than 1% of the potential distribution
area is protected by strong regulatory measures (e.g., national parks and natural reserves). The knowledge
obtained in this study allows us to recommend some guidelines that would favor the conservation of this
species.
Résumé.—Le lezard ocellé, Timon lepidus (Daudin 1802), occupe les regions méditerranéennes du sud-ouest
de l’Europe (Portugal, Espagne, France, et extréme nord-ouest de I’Italie). Au cours des derniéres décennies,
un fort declin des populations a été observe, particulierement aux marges nord de sa distribution. Il est donc
considéreé comme une espece menacée, spécialement en France et en Italie. En France, il bénéficie d’un
plan national d’actions en faveur de sa preservation. La modélisation de sa distribution a ete conduite sur
l'ensemble du territoire national en vue d’estimer sa distribution potentielle, préciser sa niche écologique,
orienter les prospections futures et permettre une meilleure prise en compte de Il’espece dans l’aménagement
du territoire. Le travail de modelisation repose sur 2757 points d’observation répartis sur l’?ensemble de la
distribution connue de l’espéce, confrontes a 34 variables climatiques, topographiques, et de couvert vegetal.
Apres suppression des variables autocorrélées, plusieurs combinaisons de variables ont éte testees, et leur
performances évaluées a partir de huit algorithmes SDM. Le meilleur modele retient neuf variables, déterminees
par l’algorithme ayant la meilleure performance. Les modeles montrent que la presence de l’espéce est
Correspondence. ':*p.jorcin@naturalia-environnement.fr, ?1.barthe@natureo.org, * matthieu.berroneau@cistude.org,
*florian.dore@gmail.com, ° Philippe.geniez@cefe.cnrs.fr, ° p.grille(@wanadoo fr, ’ benjamin.kabouche@lpo.fr, *alexandre.movia@lpo.fr,
*naimi.b@gmail.com, '° g.pottier@natureo.org, |! thirion.jean-marc@sfrfr, '* marc.cheylan@cefe.cnrs.fr
Amphib. Reptile Conserv. 276 December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
principalement déterminée par la sécheresse et la température estivale: précipitations au cours du mois le
mois le plus sec, saisonnalite des précipitations et temperature moyenne des trois mois les plus chauds. La
validation du modele sur la base d’un échantillon totalisant 25 % du total des observations, non inclus dans le
modele, montre que 94 % des données de validation se placent dans I’aire potentielle au seuil de probabilite de
0,7, et 90 % pour une probabilité comprise entre 0,8 et 1. Ceci donne une valeur predictive tres elevee au modeéle
retenu. On constate une étroite concordance entre la distribution potentielle et la distribution réalisée, ce qui
suggere une faible influence des facteurs géographiques (obstacles a la dispersion), historiques (processus
de dispersion) ou ecologiques (competition, ressources trophiques, etc.). Le croisement cartographique entre
l’aire potentielle de ’espece et les espaces protéegés montre que moins de 1 % de Il’aire potentielle est couverte
par des mesures réglementaires fortes (parcs nationaux et reserves naturelles). En conclusion, le travail donne
des orientations pour ameéliorer la connaissance de la distribution de l’espece et des pistes de réflexion en
faveur de sa conservation.
Keywords. Timon lepidus, species distribution models, ecological niche, Europe, Reptilia, Sauria, Squamata
Citation: Jorcin P, Barthe L, Berroneau M, Doré F, Geniez P, Grillet P, Kabouche B, Movia A, Naimi B, Pottier G, Thirion J-M, Cheylan M. 2019.
Modelling the distribution of the Ocellated Lizard in France: implications for conservation. Amphibian & Reptile Conservation 13(2) [General Section]:
276-298 (e213).
Copyright: © 2019 Jorcin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 11 December 2018; Accepted: 23 August 2019; Published: 22 December 2019
Introduction
The success of conservation programs in protecting
threatened species depends largely on the quality of
the information related to the environmental condi-
tions favorable to (or sought by) the species (Griffith et
al. 1989; Souter et al. 2007; Fourcade et al. 2018). For
this reason, ecological (or environmental) niche mod-
els (ENMs) [Sillero 2011], also known as species dis-
tribution models (SDMs) or habitat distribution models
(HDMs), are increasingly used to inform conservation
measures (Ferrier 2002; Graham et al. 2004; Araujo and
Segurado 2004; Santos et al. 2009; Elith and Leathwick
2009; Lyet et al. 2013; Jiang et al. 2014; Wan et al. 2016:
Tanella et al. 2018). These models allow researchers to
identify the factors which explain the distribution of a
species (Austin et al. 1990; Vetaas 2002; Guisan and
Hofer 2003; Jiang et al. 2014; Ferreira et al. 2013), to
orient research toward zones where the species has not
yet been identified (Engler 2004; Raxworthy et al. 2003;
Lyet et al. 2013; GHRA-LPO Rhone-Alpes 2015; Ryberg
et al. 2017), to identify the most favorable zones for the
conservation of the species (Brito et al. 1996; Barbosa
et al. 2003; Anderson and Martinez-Meyer 2004; Mufioz
et al. 2005; Guisan et al. 2013; Lyet et al. 2013; Wang
et al. 2016; Moradi et al. 2019; Sohrab et al. 2019), to
evaluate the potential dispersion and gene flow between
population patches (Guisan and Thuiller 2005), to model
future changes in distribution (for example, based on cli-
mate change) [Franklin 1998; Guisan and Hofer 2003;
Araujo et al. 2006; Carvalho et al. 2011; Cheaib et al.
2012; Ianella et al. 2018; Renwick et al. 2018], as well as
to project the distribution into past scenarios (Sillero and
Carretero 2013).
Species distribution models also allow comparisons
Amphib. Reptile Conserv.
between potential and actual distributions, two very use-
ful concepts to consider in conservation biology. Put sim-
ply (see Pulliam 2000 for a more detailed explanation),
a potential niche corresponds to areas in which the cli-
matic, terrain, and habitat conditions are theoretically fa-
vorable to the species in the current conditions, whereas
the realized niche takes into account historical and bi-
otic factors that may explain the absence of the species
within the ecological area defined by the fundamental
niche. Comparing these two niches provides informa-
tion about the historical processes that led to the cur-
rent distribution, the dispersion capacity of the species,
and the obstacles to its dispersion. This can illuminate
the ecological factors that negatively influence the pres-
ence of the species, such as the presence of competitors
or predators, unsuitable habitats, insufficient trophic re-
sources, a lack of host species, and others (see Guissan
and Thuiller 2005). When used to model the distribution
of a species in decline, SDMs can also provide informa-
tion about the causes of decline, particularly by helping
to differentiate the proportions due to global factors as
opposed to regional or local factors (Jiang et al. 2014). In
some cases, SDMs can even allow the extent of decline
to be measured, by comparing the potential niche with
the observed niche (Lyet et al. 2013; Ryberg et al. 2017).
The Ocellated Lizard, Timon lepidus (Daudin 1802),
is a good case study for this type of analysis. This species
occupies the Mediterranean regions of southwestern Eu-
rope (Portugal, Spain, France, and the extreme northwest
of Italy) [Figs. 1 and 2]. At the edges of its distribution,
it has faced a marked population decline over the last de-
cades and is now considered a threatened species, espe-
cially in France and Italy (Salvidio et al. 2004; Cheylan
and Grillet 2005; Cheylan 2016).
This species is closely linked to the Mediterranean
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Jean Nicolas.
climate and specific biotopes (Doré et al. 2015). More-
over, due to its large size and thermal requirements for
reproduction, it 1s particularly demanding regarding cli-
matic conditions (Mateo 2011). The incubation period
for its eggs is long, about 100 days, making use of the
full period of warmer temperatures. The eggs hatch late,
generally at the end of September or the beginning of
October (Bischoff et al. 1984; Doré et al. 2015). Hence,
two main factors drive the distribution of this species: its
ecophysiology (thermal requirements linked to the indi-
vidual’s bulk and to the incubation of the eggs) and its
habitat requirements (dry habitats with little tree cover).
In view of these needs, the Ocellated Lizard should theo-
retically benefit from the warming temperatures recorded
in Europe over the last 30 years (see Prodon et al. 2017).
Yet observations show a rather widespread decline of this
species, particularly on the northern edge of its distribu-
tion range, which is inconsistent with the expected situa-
tion in warming conditions (Salvidio et al. 2004; Cheylan
and Grillet 2005; Doré et al. 2015). This raises questions
regarding the causes of the decline of this species and, at
first glance, suggests a hypothesis that local effects pre-
dominate over global effects.
The use of SDMs allows the study of interesting bio-
geographical questions about this species. Native to the
Iberian Peninsula, the Ocellated Lizard colonized France
and the extreme west of Italy along the Mediterranean
coast (Sillero et al. 2014; Doré et al. 2015). This colo-
nization involved overcoming considerable physical ob-
stacles, including rivers, mountains, and forests. Niche
modelling can provide information about constraints that
limit dispersion; that 1s, whether the current distribution
boundaries of the species are of a climatic nature (thus
ecophysiological) or a physical nature (due to obstacles
to dispersion). The same question applies to the species’
colonization of the French Atlantic coast: Are the isolat-
ed populations along this coast the result of a process of
decline linked to the progressive degradation of habitat
or to climatic constraints? The responses to these ques-
tions can be found by comparing the expected distribu-
Amphib. Reptile Conserv.
Fig. 2. Timon lepidus, juvenile, Hérault, France. Photo by Jean
Nicolas.
tion with the observed distribution; that is, by comparing
the potential niche with the realized niche.
This study used species distribution modelling to 1n-
vestigate the following questions: (1) Does the observed
distribution of the Ocellated Lizard match its potential
distribution? If not, why not? (2) Which variables best
explain the distribution of this species: climate, terrain,
land use, or other factors? (3) Why is this species retreat-
ing at the edges of its distribution range, in contrast to
what might be expected based on climatic changes? (4)
Are the distribution boundaries of this species conditional
on either climate, physical barriers, or ecological causes?
(5) Which zones are potentially the most favorable for
the conservation of this species? (6) Where should future
surveys be carried out to improve our understanding of
the distribution range? (7) Based on these findings, what
conservation strategy should be implemented for the
conservation of the species?
Materials and Methods
Data
Ocellated Lizard dataset. This study used observations
(presence data only, Brotons et al. 2004) from an exhaus-
tive database that includes most of the occurrences ob-
served in France between 1970 and 2016. As the objec-
tive was essentially practical, 1.e., to identify the areas
of the potential presence of the species with the aim of
its conservation, this study did not consider taking into
account the entire distribution of the species as relevant
to building the model. This would have led to further
complications, such as the need to consider markedly di-
vergent genetic lines and, as a result, ecophysiological
adaptations specific to the regions that host these genetic
lines.
The data were collected by a number of organizations
and individuals over a period of 46 years. Before inte-
grating the data into the models, the records were verified
and cross-validated, keeping only precisely georefer-
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
02550 100km
Fig. 3. Localization of the total presence data for the Ocellated Lizard Timon lepidus collected in Fran
2016.
enced locations (either data captured by GPS or observa-
tions recorded with a spatial positioning error of less than
100 m). This resulted in presence data for a total of 5,521
locations spread over southern France. From this, a sam-
ple dataset was extracted for modelling purposes. First,
only occurrences for the period that corresponded to the
vegetation variable used in the model were selected, tak-
ing into account the development and continuity of the
vegetation cover over the years. To fit this requirement,
the presence data were narrowed down to a sourcing pe-
riod of 16 years, which included 4,282 observations from
2000 to 2016. The distribution of occurrence data for this
period covers the whole area of study, though data prior
to the year 2000 were not included (Fig. 3).
Secondly, the dataset was filtered to avoid spatial bias
due to oversampling at particular locations, as field in-
vestigations conducted for environmental impact assess-
ments and other monitoring programs led to a higher con-
centration of data at certain sites. Therefore, the density
of points per km? was evaluated to identify zones subject
to sampling bias (Fig. 1 in Supplementary Materials),
using kernel density calculation. Through this analysis,
zones where the point density ranged from 2—50 points
per km? were determined, and for these zones, a single
record was retained per km?. After filtering the data by
density, a total of 2,757 occurrences were retained, pro-
viding presence data that was well distributed over the
study area (Fig. 4). Finally, of these 2,757 valid records,
75% were randomly selected for modelling, with the re-
maining 25% serving as an independent source to check
(validate) the results (Hirzel and Guisan 2002) [Fig. 4].
During the modelling procedure, the database consisting
Amphib. Reptile Conserv.
ane) a, HERE Dy
JET) Eee tran (hing
@ Presence data collected 1970-1999 (1,239 points)
® Presence data collected 2000-2016 (4,282 points)
5 MAAN, Cede ay. Ean tage
shai Eu CHES Uae Ce
ce during the period 1970 to
of 75% of the occurrences was itself divided into training
data (80%) and testing data (20%).
Environmental data. A set of ecogeographical variables
was used to model species distribution, taking into ac-
count the ecological requirements of the species (Guisan
and Thuiller 2005). A group of 34 variables was evalu-
ated through several iterations in order to identify and
include the most relevant variables (Table 1).
As a first step, environmental variables were obtained
from available sources at the appropriate spatial and the-
matic resolutions. This study used the CHELSA data-
base, version 1.1 (Climatologies at High Resolution for
the Earth’s Land Surface Areas, Karger et al. 2017). This
database includes a set of bioclimatic variables, with
monthly mean temperature and precipitation patterns,
for the time period 1979-2013, which corresponds to the
time range of the species occurrence data. The CHEL-
SA database is an alternative source to the widely used
WorldClim global climate database, as both derive their
bioclimatic variables from the monthly minimum, maxi-
mum, and mean temperatures, as well as precipitation
values. However, as described by Karger et al. (2017),
the CHELSA variables include additional corrections,
such as monthly mean and station bias, wind effect and
valley exposition, as well as correction for orographic
effects on precipitation. Additionally, as CHELSA is a
recently released product, this study allowed evalua-
tion of its potential for species distribution modelling.
In a recent study, Karger et al. (2017) highlighted differ-
ences observed at a large scale between WorldClim and
CHELSA models, with the latter leading to a significant
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
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25% of occurence data used
for validation
i, HERE, DeLorme, Intermap, increment P Ci
China (Hong Kong), swisstopo, Mapmy!ndia, @
Fig. 4. Localization of occurrence data for the Ocellated Lizard Timon lepidus, showing the points in the dataset used for the model
(red) and those used to check the model (blue).
improvement in SDM performance. The CHELSA bio-
clim data grid has a 30-arc-second pixel resolution, cor-
responding to a spatial resolution of 0.00833 decimal de-
grees at the equator. Applied to the study area in southern
France, the bioclimatic variables have a spatial resolution
of less than 1 km’, with each grid roughly covering an
area of 700 x 900 m.
As the CHELSA database does not include variables
reflecting solar radiation and its impact on climatic hu-
midity or aridity, data produced by the Consultative
Group on International Agricultural Research (CGIAR)
were used (Fick and Hiymans 2017). Data available at the
same resolution as the CHELSA dataset included mean
annual solar radiation, potential evapotranspiration, and
a global aridity index calculated from the ratio of mean
annual precipitation to mean annual potential evapo-
transpiration.
During the process of selecting and consolidating the
ecogeographical variables, another climate data source
was used to compare the results and identify the best input
that would optimize performance. This climate dataset
(Joly et al. 2010) is based on data from Meétéo France’s
weather stations and gathers a number of indicators that
are not provided in the CHELSA dataset, such as the
number of days with a temperature above 30°C or below
-5 °C, as well as other parameters related to temperature
ranges and seasonal variations over the year.
To increase model performance, topographic data
were also included. The elevation was obtained from the
EU-DEM v1.1 dataset, produced in the framework of
the European Commission’s Copernicus program (Bash-
field and Keim 2011), which includes a digital elevation
Amphib. Reptile Conserv.
model captured in 2011 and projected in ETRS89-LAEA
(EPSG code 3035), with a spatial resolution of 25 m.
This allowed the modelling to take altitude into account,
as well as slope and aspect, calculated in projected coor-
dinate systems (all in meters).
A variable representing vegetation cover is also re-
quired, in order to identify natural habitats suitable for
the Ocellated Lizard. The vegetation cover indicator se-
lected was the normalized difference vegetation index
(NDVI) generated from the MODIS (Moderate resolu-
tion Imaging Spectro-radiometer) Terra satellite sensors
(Huete et al. 2010), which has a spatial resolution of 250
m. Data captured in the first week of July were used, as
this corresponds to the optimal season for identifying
the permanent vegetation cover of interest in this study.
Vegetation indices in summer can highlight chlorophyll
produced by permanent vegetation, whereas vegetation
indices calculated in spring are influenced by the annual
growth of the herbaceous stratum.
Considering the possibility that land cover has
changed over time, the importance of changes in veg-
etation cover over the years was evaluated. The NDVI
values were compared for each year from 2000 to 2016,
calculating the variance and the standard deviation of
the mean NDVI value for this 16-year period (Fig. 5).
The results indicated that the change in permanent veg-
etation cover in the area of interest has been negligible,
especially in areas where the Ocellated Lizard has been
observed. Over 16 years, for the month of July, the stan-
dard deviation of the yearly NDVI values relative to the
NDVI mean value was below 0.075 for 98.9% of the en-
tire studied area, below 0.05 for 88.9% of the area, and
280 December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
Table 1. Description of the 34 variables evaluated.
Variable Description Source Period Resolution
Biol Annual mean temperature CHELSA v1.1 1979-2013 ~1 km?
Bio3 Isothermality (BIO2/BIO7) (* 100) CHELSA v1.1 1979-2013 ~1 km?’
Bio4 Temperature seasonality (standard deviation *100) CHELSA v1.1 1979-2013 ~1 km?
Bio5 Max temperature in warmest month CHELSA v1.1 1979-2013 ~1 km?’
Bios Mean temperature in wettest quarter CHELSA v1.1 1979-2013 ~1 km?
Bio9 Mean temperature in driest quarter CHELSA v1.1 1979-2013 ~1 km?’
Biol0 Mean temperature in warmest quarter CHELSA v1.1 1979-2013 ~1 km?
Biol3 Precipitation in wettest month CHELSA v1.1 1979-2013 ~1 km?
Biol4 Precipitation in driest month CHELSA v1.1 1979-2013 ~1 km?’
Biol5 Precipitation seasonality (coefficient of variation) CHELSA v1.1 1979-2013 ~1 km?
Biol6 Precipitation in wettest quarter CHELSA v1.1 1979-2013 ~1 km?’
Biol7 Precipitation in driest quarter CHELSA v1.1 1979-2013 ~1 km?
Bio 18 Precipitation in warmest quarter CHELSA v1.1 1979-2013 ~1 km?’
Biol9 Precipitation in coldest quarter CHELSA v1.1 1979-2013 ~1 km?’
EU-DEM v1.0 European
Alt Elevation Commission Copernicus program 2011 25m
Slope Slope Calculated from EU-DEM v1.0 2011 25m
Aspect Slope orientation Calculated from EU-DEM v1.0 2011 25m
NDVI Normalized vegetation index MODIS TERRA (NASA) July 2012 250m
TCD Tree cover density Copernicus 2012 20m
srad Mean annual solar radiation WORLDCLIM v.2 1970-2000 ~1 km?’
PET Global potential evapotranspiration CGIAR 1950-2000 ~1 km?
Global aridity index (mean annual precipitation / mean
Aridity annual PET) CGIAR 1950-2000 ~1 km?
TMO Annual mean temperature ThéMA - CNRS-UMR 6049 1971—2000 250m
TMN Number of days with temperature below -5 °C ThéMA - CNRS-UMR 6049 1971-2000 250m
TMX Number of days with temperature above 30 °C ThéMA - CNRS-UMR 6049 1971-2000 250 m
TAM Annual temperature range ThéMA - CNRS-UMR 6049 1971—2000 250m
TEH Inter-annual temperature variability in January ThéMA - CNRS-UMR 6049 1971—2000 250 m
TEE Inter-annual temperature variability in July ThéMA - CNRS-UMR 6049 1971—2000 250 m
Variance between January precipitation and monthly mean
PDH precipitation ThéMA - CNRS-UMR 6049 1971-2000 250 m
Variance between July precipitation and monthly mean
PDE precipitation ThéMA - CNRS-UMR 6049 1971-2000 250 m
PJH Number of rainy days in January ThéMA - CNRS-UMR 6049 1971—2000 250m
PEH Inter-annual precipitation variability in January ThéMA - CNRS-UMR 6049 1971—2000 250 m
PEE Inter-annual precipitation variability in July ThéMA - CNRS-UMR 6049 1971—2000 250 m
Variation between autumn (September and October) and
PRA July precipitation ThéMA - CNRS-UMR 6049 1971-2000 250 m
only reached a maximum of 0.2 for 1.1% of the area. An
assessment of the changes in vegetation cover within the
Methodology
study area allowed the selection of the NDVI mean value
for the 16-year NDVI dataset (from 2000 to 2016).
All the selected variables were aggregated to a spa-
tial resolution of ~1 km, using bilinear resampling tech-
niques.
Amphib. Reptile Conserv. 281
The performance of models was explored based on dif-
ferent combinations of ecogeographical variables using
an iterative approach (Heikkinen et al. 2006). To do this,
a model was first fitted with a selected set of variables
(Bucklin et al. 2014) and its performance was measured.
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Table 2. Input variables for the six models. See Table 1 for descriptions of variables.
Code Model description
M1 six selected bioclimatic variables
M2 eight random bioclimatic variables (blind test)
M3 12 climatic variables from Météo France
M4 M1 variables + solar radiation + PET + aridity
M5 M1 variables + altitude, slope, aspect
M6 M1 variables + altitude, aspect + vegetation
The inputs were then optimized by testing the model with
other sets of variables, using a stepwise procedure to 1n-
clude or exclude variables one by one. Every iteration
was evaluated and outcomes associated with the chosen
parameters were recorded. This resulted in six models
based on different combinations of variables (Table 2).
While a comparison of bioclimatic data sources in
terms of usefulness for species distribution modelling is
beyond the scope of this study, a deliberate choice was
made to use various sources in the model; specifically,
bioclimatic data from entirely different inputs. This itera-
tive and multiple-source approach increases the chances
of obtaining a successful model by allowing the selection
7 heey | see,
peek ta Se : x
cee | ga fai hy
ee Eee ‘
0 2550 100km
| | |
Source: The standard deviation of yearly NDVI relative to the mean NDVI
for the month of July was calculated from MODIS data captured on the first
week of July every year from 2000 to 2016.
Variables
Bio4, Bio9, Biol0, Biol4, Biol5, Biol6
Bio3, Bio4, Bio5, Bio8, Bio9, Biol3, Biol7, Biol9
TMO, TMN, TMX, TAM, TEH, TEE, PDH, PDE, PJH,
PEH, PEE, PRA
[Biol, Bio4, Bio9Bio15, Biol6] + srad + PET + Aridity
[Bio4, Bio9, Biol0, Biol4, Biol5, Biol6] + Alt, Slope,
Aspect
[Bio4, Bio9, Biol0, Biol4, Biol5, Biol16] + [AIt, Aspect]
+ NDVI
of the most accurate and relevant variables. It also helps
to validate overall model performance, by providing keys
for analyzing the suitability of the model in terms of bio-
climatic variables favorable to the species.
Model descriptions
Model 1: Variables selected from the CHELSA climate
dataset based on ecological assumptions. The first
modelling trial used a set of ecogeographical variables
identified based on expert knowledge of the biology
and behavior of the species. As the Ocellated Lizard is a
Mediterranean species that prefers long periods of warm
Vegetation cover variation from 2000 to 2016
Standard deviation of yearly NDVI relative to the
mean NDVI for the month of July
[JO - 0.01
[10.01 - 0.05
0.05 - 0.075
0.075 - 0.1
M0.1-0.2
- Occurence data from 2000 to 2016
Fig. 5. Change in vegetation cover from 2000 to 2016: standard deviation of the yearly NDVI values relative to the NDVI mean
value for the month of July.
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e213
Table 3. Variable correlation values for Model 1.
Jorcin et al.
bio4 R bio9 R biol0_R biol4 R biol5_R biol6 R
bio4 R 1.00000000 -0.07440553 0.3081616 -0.2788248 0.1672821 -0.2605788
bio9_R -0.07440553 1.00000000 0.5115825 -0.4025089 0.3664137 -0.0604624
biolO_R 0.30816159 0.51158248 1.0000000 -0.6782349 0.6210210 -0.1046921
biol4 R -0.27882481 -0.40250891 -0.6782349 1.0000000 -0.6896546 0.2434781
biolS_R 0.16728213 0.36641372 0.6210210 -0.6896546 1.0000000 0.2159100
biol6_R -0.26057884 -0.06046240 -0.1046921 0.2434781 0.2159100 1.0000000
temperatures (for ecological reasons linked to its repro-
ductive cycle), this model considered the bioclimatic
variables that would best represent this need. Variables
with a recognized influence on a species’ ecology are
generally expected to lead to more accurate predictions
in SDMs (Austin 2002). This initial SDM incorporated
the following variables from the CHELSA database:
Bio4, Bio9, Biol0, Biol4, Biol5, and Biol6 (Table 3).
The Biol16 variable was selected as it represents precipi-
tation in the wettest quarter, so it would be a good in-
dicator of the aridity of the environment. This variable
differentiates regions according to precipitation patterns
by indicating rainfall occurring during the wettest period
of the year, thus allowing locations with lower rainfall
to be identified. After this a priori selection, the correla-
tions between variables were measured (Table 3). As the
variables were not correlated, this choice was validated.
Model 2: Non-correlated variables selected from the
overall CHELSA climate dataset. For the next model, the
correlations between the 19 variables obtained from the
original CHELSA database for all presence-data loca-
tions were calculated, removing one of each pair of high-
ly correlated variables (those with a correlation coeffi-
cient greater than 0.75) [Doorman 2012]. As 11 of the 19
input variables were correlated, only the remaining eight
were retained, with no consideration of any presumed
ecological significance. Thus, this trial was considered
a blind test, run on a statistical basis only rather than on
prior knowledge of the input variables. Problems of col-
linearity between variables were identified and dealt with
using variance inflation factors (VIF) with the R usdm
package (Naimi et al. 2014). A VIF was calculated for
each explanatory variable, and those with a VIF greater
than 10 were removed. The correlation coefficients of
the remaining variables ranged between -0.015 and 0.75
(Table 1 in Supplementary Materials).
Model 3: Non-correlated variables from the Meétéo
France climate dataset. As an alternative to the CHEL-
SA climate database, this model used a climate dataset
obtained from Météo France weather stations (Joly et al.
2010). Correlation tests showed that out of 14 variables
from the Météo France dataset, only two were highly
correlated, with a correlation coefficient greater than
0.75. Therefore, the 12 non-correlated variables were in-
cluded in the model, with each having a potential effect
on model performance.
Amphib. Reptile Conserv.
Model 4: The variables for Model I with the addition
of solar radiation, evapotranspiration, and aridity.
This model included the six climate variables selected
for Model | in addition to climatic parameters that are
potentially important to the ecology of the species. To
reflect discriminating factors related to the Mediterra-
nean climate, this model used mean annual solar radia-
tion (obtained from WorldClim), as well as the Global
Potential Evapotranspiration and Global Aridity Index
(obtained from CGIAR) [Fick and Hijmans 2017]. The
Global Aridity Index consists of mean annual precipita-
tion divided by mean annual potential evapotranspiration
(Zomer et al. 2008). An assessment of whether the per-
formance of the model increased with these additional
variables was made.
Model 5: The variables for Model I with the addition
of topographic variables. This model included the six
climate variables selected for Model 1 along with three
additional topographic variables: elevation, slope, and
aspect (orientation). Topographic parameters were ex-
pected to improve model performance (Humboldt and
Bonpland 1805).
Model 6: The variables for Model I with the addition
of selected topographic variables and a vegetation
variable. The final model included the six climate vari-
ables selected for Model 1 along with two additional
topographic variables (elevation and aspect) as well as
NDVI. The two topographic parameters were retained
because of the gain in performance obtained by add-
ing them to the bioclimatic parameters. The addition of
the NDVI helped to account for vegetation cover as a
contributing variable in the model, as this is a valuable
parameter in identifying the natural habitat of the spe-
cies. Assuming the distribution of the Ocellated Lizard
is linked to this species’ preferences in terms of land
cover, vegetation density is expected to help differenti-
ate areas of occurrence from areas of absence (Wilson
etal 2013),
SDM methods
To maximize SDM accuracy, all six models were run
with eight statistical algorithms (Bucklin et al. 2014),
regression-based machine learning, and classification
methods. With each algorithm resulting in different pre-
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Table 4. Algorithms used in the species distribution modelling.
Code Description
BRT Boosted Regression Trees
CART Seek rae Regression Trees for
GAM Generalized Additive Model
GLM Generalized Linear Model
MARS Multivariate Adaptive Regression Spline
MAXLIKE Maximum Likelihood
RF Random Forests
SVM Support Vector Machine
dictions, the objective was to identify the method that
achieved the best accuracy (Elith et al. 2006). Testing
eight algorithms also allowed the evaluation of the over-
all modelling approach (Table 4). As well as analyzing
discrepancies between models in terms of performance,
model congruence was examined to consolidate the
conceptual approach (Li and Wang 2012). The model-
ling methods used were Generalized Linear Modelling
(GLM, Guisan and Zimmerman 2000), Generalized Ad-
ditive Modelling (GAM, Guisan and Zimmerman 2000),
Multivariate Adaptive Regression Spline (MARS, Elith
and Leathwick 2007), Maximum Likelihood (MAX-
LIKE), Classification and Regression Trees for Machine
Learning (CART, Breiman et al. 1984), Boosted Regres-
sion Trees (BRT, Elith et al. 2008), Support Vector Ma-
chine (SVM, Drake et al. 2006), and Random Forests
(RF, Breiman 2001).
The presence-absence models were used with the ob-
jective of predicting the presence probability of the Ocel-
lated Lizard and mapping its distribution accordingly.
Lacking absence data, pseudo-absences were used to
run the models. Pseudo-absence data was generated with
the R sdm package (Naimi and Araujo 2016), which has
the advantage of providing a pseudo-absence selection
process calibrated to SDM performance by considering
presence data. Other studies have found that randomly
selected pseudo-absences yield the most reliable models
(Barbet-Massin et al. 2012). The models were fit by as-
signing a number of pseudo-absences weighted to pres-
ences (Barbet-Massin et al. 2012), with an equal number
of presences and absences.
Each type of SDM methodology has particular strengths
and limitations in the way it accommodates the responses
to predictors, as well as how it deals with missing observa-
tions. For example, linear regression fits linear functions
relating a response variable to one or more predictor vari-
ables, where this relationship can be approximated by a
straight line (Ferrier et al. 2002), whereas machine learn-
ing offers more complex classification algorithms that
accommodate non-linear variable interactions (Salas et
al. 2017). All algorithms were tested with replicated sub-
sampling of 20% of the occurrence dataset.
Amphib. Reptile Conserv.
Model evaluation methods
The contribution of SDMs in understanding the
geographical distribution and abundance of a species
depends on the level of reliability offered by the model
(Barry and Elith 2006). The prediction accuracy must
be assessed to determine the model’s suitability (Liu
et al. 2009). Models can be judged on their capacity to
discriminate presence from absence, which is measured
by the number of false positive and false negative
predictions. Several statistical indicators can be used as
metrics to evaluate model performance (Fielding and
Bell 1997). To assess the results here, the area under the
Receiver Operating Characteristic (ROC) curve (AUC)
value was used, as well as the correlation coefficient
(COR) and the True Skill Statistics (TSS) value (Bradley
1997). The AUC value provides a single measure of
model performance, showing the model’s ability to
rank a randomly chosen presence observation higher
than a randomly chosen absence observation (Liu et
al. 2009). These values can range between 0 and 1; and
models producing AUC values of 0.75 are regarded as
reliable, 0.8 as good, and 0.9 to 1 as having excellent
discriminating ability (Franklin 2009). The TSS is
presented as an improved measure of model accuracy,
defining the average of the net prediction success rates
for presence sites and for absence sites (Allouche et al.
2006). The COR value allows another performance index
comparison between models, and helps to validate the
results obtained by the AUC and TSS methods (Elith et
al. 2006). This study also ran null models, which make
predictions in the absence of a particular ecological
mechanism (Harvey et al. 2003), to assess the random
probability hypothesis. The AUC values from the null
models ranged from 0.51 to 0.53, thus corresponding to
what would be expected by chance (Raes and ter Steege
2007). The distribution generated with a null model
significantly differed from the other modelling results,
with a predicted presence spread smoothly over most of
the study area (Fig. 2 in Supplementary Materials).
As well as evaluating model performance with
statistical indicators, the results were checked against
the validation dataset (Anderson et al. 2003), consisting
of the 25% of available presence data set aside for
validation. The data distribution showed that 76%
of the observation records within the presence range
correspond to a threshold value of 0.9 to 1, and 86% were
above a threshold of 0.8 (Table 5). Of the 690 occurrence
locations set aside to check the results, 92% fell within
the area predicted by the modelled map, in line with a
presence probability threshold of 0.70.
Predictive maps generated by SDMs provide the oc-
currence probability of the species on a 0 to 1 scale.
Threshold determination is a key step in transforming 1n-
dices of suitability to binary predictions of species pres-
ence or absence (Nenzen and Araujo 2011). Threshold
definition can be subjective or objective (Manel et al.
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
Table 5. Correspondence between observations and presence
probability for the validation dataset. Values above a threshold
of 0.7 are shown in bold.
Probability threshold Sonate -
0.9 to 1 2,219 80.4
0.8 to 0.9 266 9.7
0.7 to 0.8 114 4.1
0.6 to 0.7 80 20
0.5 to 0.6 43 ne
0.4 to 0.5 13 a
0 to 0.4 22 ue
1999), and in many methods, the point at which sensitiv-
ity (true positive rate) and specificity (true negative rate)
are equal can be chosen to determine the threshold. In
this case, a value of 0.7 was chosen.
Results
All SDMs for the differing sets of variables performed
well, demonstrating high predictive power (Table 6). The
overall mean AUC value was 0.86, the mean TSS was
0.67, and the mean COR was 0.61. These results con-
firmed the hypothesis that SDMs based on bioclimatic
variables could provide valuable results for the Ocel-
lated Lizard. Moreover, the agreement between results
validates the overall modelling methodology, including
the quality of the sampling dataset and the geographical
extent of the study. Overall, the initial trial made with
Model 1 showed that it was a satisfactory model, with
an AUC value of 0.91, a TSS value of 0.72, and a COR
value of 0.78. The subsequent iterative trials carried out
with different combinations of variables further increased
model accuracy, validating the most useful variables and
helping to rank their contributions.
A comparison of the overall results led to the selection
of Model 6 generated with the RF method as the most
accurate model. The predictors of this model, based on
selected bioclimatic variables with additional topograph-
ic and vegetation parameters, achieved the best perfor-
mance using virtually all modelling methods, with maxi-
mum performance obtained from the RF method. This
combination of variables and modelling method resulted
inan AUC value of 0.98, a TSS value of 0.85, and a COR
value of 0.88. An analysis of variance (ANOVA) was
performed to confirm the validity of the chosen combina-
tion of variables. ANOVA results on Model 6 showed the
lowest p-values for all variables, with a minimum value
of 2.74e-14 and a maximum value of 0.020393 (Table 7).
In contrast, models 1 to 5 each included a variable with
a p-value > 0.05. As a study by Wood et al. (2016) men-
tioned that the Akaike information criterion (AIC) works
reasonably well for model selection, the AIC between
models were also compared here, and this comparison
showed that Model 6 had the lowest AIC values (Table 2
in Supplementary Materials).
Contribution of Variables
The contributions of each variable in Model 6 were
ranked, identifying four critical parameters, as well as
one secondary factor (Table 8). The four main factors
that most influenced model performance were (according
to their relative importance): precipitation in the driest
month, temperature seasonality, mean temperature 1n the
driest quarter, and NDVI. Precipitation seasonality was
Table 6. Comparison of model results based on different modelling methods and assessments of model performance. The values in
bold, for Model 6 and RF, indicate the results with the highest accuracy.
x [os [aie
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[auc [cor [1s [auc | cor [ 18s | auc | cor | 1s | auc [ cor] 155
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December 2019 | Volume 13 | Number 2 | e213
Amphib. Reptile Conserv. 285
Distribution of Timon lepidus in France
N
A 0 50 100km
LJ
N mater
A? 50 100 km
Ld
N
A 0 50 100km
LJ
Presence
probability
i o-o
[_]0-0.05
[_] 0.05 - 0.1
[J 0.1 - 0.15
[0.15 - 0.2
[9 0.2 - 0.25
[) 0.25 - 0.3
fl 0.3 - 0.35
[i 0.35 - 0.4
I) 0.4 - 0.45
i 0.45-0.5
Ml 0.5 - 0.55
Ml 0.55-0.6
MM 0.6 -0.65
Hl 0.65 - 0.7
i 0.7 - 0.75
MW 0.75-08
MH o8-0.85
MM 085-09
MM 0.9-0.95
MM 0.95-1
MODEL 4
N
A 0 50 100 km
—
Fig. 6. Predictive modelling maps showing presence probability of the Ocellated Lizard (Timon lepidus) in the study area.
also a contributing variable, but only to a minor extent.
Climatic factors associated with dry and warm weather
conditions seem to play a determining role in the spatial
distribution of the Ocellated Lizard, with precipitation in
the driest month being the primary contributing factor.
The contributions of these variables can be interpreted as
a reflection of the species’ ecological needs, especially as
related to its reproductive cycle.
Predictive Habitat Suitability Maps
The predictive maps (Fig. 6) show very slight differences
between the six models. Oléron Island, where the most
northerly currently known population of this species is
found, is included in all models, but with different prob-
ability ranges. Its presence is predicted on the whole is-
land in models 1, 2, 4, and 5, but only on part of the island
in models 3 and 6. All models show a clear link between
the ‘Mediterranean population’ and the ‘Lot population’
(in a region lying northwest of the Mediterranean), with
minor variations in the continuity of the species distri-
bution between these two ‘populations.’ In the different
maps, the penetration of the species into the Rhéne Val-
ley appears more or less extended, and the fragmentation
of the “Lot population’ is more or less pronounced. Apart
from these details, the maps based on the six models are
extremely consistent.
Amphib. Reptile Conserv.
On the map generated by Model 6 (Fig. 7), most of
the locations historically occupied by the species (1.e.,
for which evidence exists of its disappearance) are along
the Atlantic coast (in the Nouvelle-Aquitaine region), the
area where the distribution of the species 1s the most lim-
ited and fragmented (Fig. 8). The disappearances of the
three Mediterranean populations correspond to very spe-
cific cases: two islands (Ratonneau and Porquerolles is-
lands), where the species is likely to have disappeared as
a result of the introduction of predators (Cheylan 2016),
and a population in the Rhdéne delta in the Camargue,
where the decline of rabbits has transformed the envi-
ronment, leading to the disappearance of the Ocellated
Lizard in this area (Doré et al. 2015).
Identification of Knowledge Gaps
The potential distribution predicted by Model 6 indi-
cates that knowledge gaps regarding the observed pres-
ence of this species are considerable, not only in the
Mediterranean distribution range, but also in its pe-
riphery (Fig. 9). Allowing a buffer zone with a 5-km
radius around each observation location, only 74% of
the area of predicted presence (based on Model 6 with
a presence probability threshold of 0.70) is confirmed
by actual observations; observation data is lacking for
26% of the area. In the core of the distribution range,
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
nm
0 2550 100km
2
7 elicomeh
e Presence data collected 2000-2016
® Predicted distribution of Ocellated Lizard
Bi, WG, RAL NPS, RAIA, depots KIM Kaede NL. Cecnance Sucany, Ean depen
} Sapereparemn, iB ipe aD 00 a aved Tee GIS Lege Con
Fig. 7. The predicted distribution map generated by Model 6 (in pink) with specific locations of presence data (from observations)
from the dataset (black dots).
information is missing in several areas of the regions
of Provence and in a few areas of Languedoc-Roussil-
lon. This is particularly the case for several noteworthy
zones.
¢ Var department (e.g., around Fayence, Draguig-
nan, Bargemon, Seillons-source-d’Argens, and
Saint-Maximin-la-Sainte-Baume)
¢ Southeast of Alpes-de-Haute-Provence (e.g., the
Valensole plateau, the Asse-Puimichel valley,
and the lower Bléone valley)
¢ Southeast and northwest of the Vaucluse depart-
ment (e.g., Pertuis, La Tour-d’Aigues, Carpen-
tras, Uchaux, Sainte-Cécile-les-Vignes, and
Valréas)
¢ Dréme department (Valence plain, Monteéli-
mar plain, Tricastin, and Baronnies Proven-
cales)
¢ Gard department (e.g., Saint-Quentin-la-Poterie,
Bagnols-sur-Ceze, Ales, and La-Grand-Combe)
¢ Southeast of Ardeche (e.g., Saint-Thome, Vil-
leuneuve-de-Berg, and Saint-Marcel-d’ Ardeéche)
¢ South and far northwest of the Lozere (e.g.,
Aysseries, Faveyrolles, La-Bastide-Solages, Sé-
brassac, Decazeville, and Claunhac)
In western Languedoc-Roussillon, it would seem rel-
evant to look for the Ocellated Lizard in several zones
of the Aude department (e.g., Carcassonne, Labécede-
Lauragais, Rouffiac-des-Corbieres, and Palairac),
and in several areas of the Pyrénées-Orientales (e.g.,
Saint-Paul-de-Fenouillet, and La Trinité) and the
Amphib. Reptile Conserv.
Herault (e.g., Pézenas and Aigues-Vives). Outside of
the Mediterranean region, areas where this species
would merit further survey efforts are more numerous,
notably in the Aveyron, Tarn, Haute-Garonne, Tarn-et-
Garonne, Lot, and in Dordogne, where the potential
distribution area is very fragmented and the natural
habitats small (Berroneau 2012; Pottier et al. 2017).
To address this, surveys could be carried out in several
areas of the Tarn and the Lot (e.g., Mazamet, Roque-
courbe, Larroque, Lacapelle-Marival, Prayssac, Gour-
don, and Martel), in southwest Correze (e.g., Tulle,
Taurisson, and Saint-Aulaire), in southeast Dordogne
(e.g., Carsac-Aillac, Hautefort, and Rouffignac-Saint-
Cernin-de-Reilhac), and in eastern Tarn-et-Garonne
(e.g., Caylus). All of these areas possess a high pres-
ence probability of this species according to the model
results, so it 1s likely that inadequate surveying ex-
Table 7. ANOVA produced by the Generalized Additive Model
for Model 6. Approximate significance of smooth terms.
Edf Ref.df Chi.sq p-value
s(bio4_R) 7.928 8.263 84.87 2.74e-14
s(bio9_R) 7.445 7353 38.47 5.88e-06
s(biol10_R) 6.469 6.779 42.75 7.37e-07
s(biol4_R) 7.608 8.248 18.61 0.020393
s(biol5_R) 6.071 7.297 18.72 0.008308
s(biol16_R) 7.944 8.688 18.79 0.018410
s(alt250_R) 6.279 6.819 34.27 9.87e-06
s(orient250_R) 3.392 4.241 20.47. ~~ 0.000507
s(median MO- 2.734 3.462 40.17 3.36¢e-08
DIS2)
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Pays _de la Loire
<— La Rochelle
Atianticfes, ff ~~ & oe epee :
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ia
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[| Regions boundaries
NN) Predicted distribution
China (Hong Keng), swisstopo, Mapmyindia, © OpenStr
Fig. 8. Location of populations that have disappeared in relation to the predicted presence map generated by Model 6 (blue dots).
plains the current absence of data in these locations.
Contribution of Protected Areas to the Conservation
of the Species
A comparison of the potential niche (Model 6 with a
presence probability of > 0.70) and the main national
protected areas allowed an assessment of the contribu-
tion of the current network of natural reserves to the con-
servation of the species (Table 9).
The map in Fig. 10 shows the protected areas that
contribute most to the conservation of the species are the
regional nature parks (representing 22% of its predicted
niche) and the two Natura 2000 zones (15% and 16%).
The other types of protected areas contribute to a much
more limited extent, covering between only 0.1% and 2%
of the potential distribution area of 35,805 km?. As these
protected areas often overlap (regional nature parks of-
ten include nature reserves, and are generally also part of
the Natura 2000 network), it 1s difficult to calculate the
surface areas to evaluate the total contribution of all the
protected sites. It should be noted that the protected areas
with the strongest regulatory protection (national parks,
national and regional nature reserves, and National For-
est Agency ecological reserves) cover less than 1% of the
potential niche of this species.
Amphib. Reptile Conserv.
Discussion
Model Performance
Nine variables, out of the selection of 28 climate vari-
ables, three topographic variables, and three vegetation
variables, were found through iteration to contribute
most effectively to the quality of the models. The tests
of six models with eight statistical algorithms led to very
sound results, confirming the performance of the models.
The consistency between the models and the statistical
soundness of the modelling are largely due to the good
spatial coverage of the source data, its geographical pre-
cision, and the size of the dataset (Araujo and Guisan
2006).
Given the exhaustive nature of the occurrence data, we
feel confident that the predictive model of the ecological
niche gives a fairly good picture of the potential distribu-
tion of the species, and can help to map its actual current
distribution. Other studies have demonstrated that SDMs
can accurately determine the natural distribution of a spe-
cies, contributing to the more complete knowledge of its
current range (Elith and Leathwick 2009).
In this study, the RF method resulted in the most accu-
rate SDMs, performing well with all the sets of variables.
This method uses decision trees based on random group-
ing of the covariates, modelling both the interactions be-
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
Table 8. Variable importance index generated by the best SDM, sorted by rank of importance.
Variable Description
biol4 Precipitation in the driest month
bio4 Temperature seasonality (std* 100)
bio9 Mean temperature in the driest quarter
ndvi Normalized Vegetation Index
biol5 Precipitation seasonality (coefficient of variation)
biol0 Mean temperature in the warmest quarter
biol6 Precipitation in the wettest quarter
altitude Elevation
aspect Slope orientation
tween the variables and their nonlinear relationships, and
it uses bootstrapping to fit individual trees (Salas et al.
2017). Cutler (2007) demonstrated that the advantages
of RF include very high classification accuracy, ability
to model complex interactions between predictor vari-
ables, and an algorithm for imputing missing values.
This gives RF the flexibility to perform several types of
statistical data analysis, including regression, classifica-
tion, survival analysis, and unsupervised learning (Cutler
2007). Rangel and Loyola (2012) also demonstrated that
machine learning methods such as RF have high statisti-
cal precision and predictive power for determining the
species distribution of well-known populations.
While the models here showed high accuracy, certain
improvements could be made by integrating additional
4 Soret Ga
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0 25.50 100km
hor
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0.1794 0.0330 1
0.1172 0.0216 2
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0.0666 0.0097 ©)
0.0335 0.0060 6
0.0394 0.0018 7
0.0575 0.0012 8
0.0219 0.0004 9
datasets not included in this study, such as soil maps, the
distribution of tree species, or detailed vegetation maps
of France (Leguédois et al. 2011). While land cover
parameters could contribute to identifying habitat suit-
ability, their integration in SDMs remains a challenge
in terms of accuracy and validity (e.g., in terms of how
current they are). The challenges of incorporating land
cover data are due to the fact that they are categorical
variables with limitations imposed by spatial resolution,
date of production, and thematic classification. Studies
have shown that continuous remotely sensed predictor
variables offer many advantages over categorical vari-
ables and can be used effectively in species distribution
modelling (Wilson et al. 2013). Models based on biocli-
matic variables have proven their efficiency in numerous
Ferrand
PUY-DE-DOME
F
SAVOIE
Nato ralde
= HAUTE-LOIRE
PNR fi i *
ARDECHE ~
- LOZERE
eee : AS
Piece
[ __] Department borders
i Predicted distribution without any
observations within 5 km
Fe Re Narr oa aera
al Predicted distribution with
observations within 5 km
Fig. 9. Areas within the potential niche of the Ocellated Lizard (in orange) for which there are no observation data (in red), based
on Model 6 with its presence probability threshold of 0.70 combined with presence data from observations including a buffer zone
with a 5-km radius.
Amphib. Reptile Conserv. 289 December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Table 9. The contributions of the different types of protected areas to the conservation of the Ocellated Lizard in France. The surface
area favorable to the presence of the species (“potential niche” in header of second column) is given in km? according to Model
M6. The percentage of the protected area relative to the total surface area of the predicted distribution range is shown on the third
column.
Surface area under protection within
Percentage of the potential
ype OUpnovectvares the total potential niche (km?) niche*
Regional Nature Park 8,121 22.68
Special Area of Conservation (Natura 2000) 5,927 16.55
Special Protection Areas (Natura 2000) 52985 15.60
National Park (park peripheral zone) 792 221
National Nature Reserve 170 0.47
National Park (park core area) 92 0.26
Ecological Reserve (National Forest Agency) 43 0.12
Regional Nature Reserve 20 0.06
* Total surface area predicted with a probability threshold of 0.7 = 35,805 km’.
studies, while one study has shown that the addition of
land cover variables to pure bioclimatic models does not
necessarily improve the predictive accuracy of the result-
ing SDM (Thuiller et al. 2004).
Consistency between Potential and Realized Distribu-
tions
The results obtained here showed strong agreement be-
tween the predictive models and the observed distribu-
tion of the Ocellated Lizard on a macro-geographic scale,
giving rise to several conclusions. The first is that climat-
ic predictors prevail over all the other predictors for this
species. The current boundaries of the distribution range
Parc’
ional
Pamplona/lruna re
National des
Saach 400 km Renae! ‘
ae Andorra = > Me
of the Ocellated Lizard in France are essentially defined
by climatic factors, which aligns with many studies on
reptiles (Guisan and Hofer 2003; Santos et al. 2009; Bri-
to et al. 2011). This suggests an ancient presence of the
Species in France, given the barriers to dispersion such as
rivers and mountains in its territory, and the time neces-
sary to colonize the entire potential bioclimatic niche. The
fragmentation of the populations at the edges of the dis-
tribution, as well as the historical information regarding
the loss of populations (Cheylan and Grillet 2005; Doré
et al. 2015), support this idea and suggest the existence
in the past of a larger and, above all, a less fragmented
range. Unfortunately, zooarchaeological information on
this subject is limited. The species is known to have been
Saint
‘Ss
tc aE aco
La Predicted distribution within
protected areas
HERE, DeLorme, Interma
METI. Esti China (Hong Kong), naa Mapi P re d icted d ist ri b utio n
outside of protected areas
Figure 10: Contribution of protected nature areas to the conservation of Timon lepidus. Predicted presence within protected areas
(dark purple) and predicted distribution range (light purple).
Amphib. Reptile Conserv.
290
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
present in France in the Middle Pleistocene (~700,000
to 150,000 yr ago), from remains in the Lazaret cave in
Nice (Bailon 2012), and remains from the Holocene have
also been found (Mateo 2011). However, the lack of fos-
sil remains from the last interglacial optimum (between
125,000 and 11,000 yr ago) does not definitively prove
the retreat of the species to the Iberian Peninsula dur-
ing this period. The presence of isolated populations on
the northern edges of the current distribution, as well as
its presence in Liguria, would have required overcoming
major obstacles (the Rhéne, Var, and La Roya rivers),
which points to an ancient occupation of the territory.
Given these factors, the hypothesis that the species re-
mained during the interglacial period seems possible, at
least in the far south of France.
The strong concurrence between the models and the
observed distribution also indicates that the process of
decline in this species is moderate, as all the areas favor-
able to the species are still occupied, apart from a few
exceptions. Even at a lower spatial resolution, the bound-
aries of the distribution range are primarily due to cli-
matic factors, and only secondarily to ecological factors
(i.e., presence of favorable habitat). This is particularly
true at the edges of its distribution range in the valleys
that open onto the Mediterranean coast (1.e., those of the
Aude, Rhéne, Durance, and Var), where the extent of the
penetration of the species coincides with the boundary
of the Mediterranean climate and vegetation, as there
are no physical obstacles preventing a deeper advance in
these valleys (Deso et al. 2011, 2015). Notably, the mod-
el clearly differentiates areas favorable to the Ocellated
Lizard in zones of rugged terrain. This is particularly the
case in the region of the Causses (in the southern part of
Aveyron), which is characterized by limestone plateaus
that would potentially be favorable to the species but
where it 1s not present, and by deep gorges (the valleys of
the Tarn and the Jonte) where the species has long been
observed. Rather surprisingly, the model distinguished
between these two zones (plateaus and gorges) despite
any notable climatic difference between them.
On the other hand, several areas not predicted by the
model have the proven presence of the species (e.g.,
the foothills of the Pyrénées in Ari¢ge, the mountain-
ous zones of Ardéche, and northern Dordogne). This is
likely explained by the resolution of the model, which is
ill-adapted to predicting very small areas within a land-
scape and climate matrix that is generally unfavorable to
the species. These known populations live in very small
micro-habitats (a few dozen ha at most) with unique
botanical characteristics distinct from the surrounding
landscapes. An analysis that takes into account a finer
landscape scale, particularly in terms of vegetation,
would produce a model with a closer fit. Equally, sub-
strate characteristics, which were not taken into account
in the model, play an important role in the presence of
the Ocellated Lizard when the climatic environment is
unfavorable. In this case, it seeks out terrain that is rather
Amphib. Reptile Conserv.
steep, rocky, or well drained to avoid environments that
are too wet.
Which Variables Best Explain the Distribution of the
Species?
At the macro-geographic scale, the variables that best ex-
plain the distribution of the species are related to climate
and, to a lesser extent, vegetation and topography. This
indicates the primacy, over all other variables, of a hot
and dry summer, as well as a strong seasonal contrast;
two key characteristics of the Mediterranean climate
(Blondel et al. 2010). The importance of temperature and
aridity in the summer Is certainly due to the reproduction
requirements of this species. In France, female Ocellated
Lizards are known to typically lay their eggs at the end
of May or the beginning of June (Cheylan and Grillet
2004), and the eggs hatch the third week of September
or the first week of October (Bischoff et al. 1984; Doré
et al. 2015). In Provence, this corresponds to an incuba-
tion period of about 100 days (Cheylan and Grillet 2004).
Hence, the entire summer period is used for reproduc-
tion. The late hatching period requires mild temperatures
at the end of summer and beginning of autumn, allow-
ing the hatchlings to feed before the hibernation period,
which begins around 15 November in most of the French
regions where this species is present (Doré et al. 2015).
At the local scale, the presence of the species 1s pri-
marily influenced by the aridity of the habitat; the Ocel-
lated Lizard prefers a rocky or well-drained substrate
that is well exposed to the sun. Dense vegetation cover
is very unfavorable for this species, as shown in a study
by Santos and Cheylan (2013) in Provence. In the future,
gaining a better understanding of the importance of each
of these habitat variables would be useful, drawing upon
the resources available on the subject.
Why is this Species Retreating at the Edges of its
Distribution Range, in Contrast to Climatic Expecta-
tions?
The proven extinction of several Ocellated Lizard popu-
lations over the last 150 years, mainly on the northern
border of its distribution range (Cheylan and Grillet
2005; Grillet et al. 2006) runs counter to what might be
expected with the warming of the climate, the effects
of which have been clearly demonstrated on Mediterra-
nean reptiles in the south of France (Prodon et al. 2017).
Given its high thermal requirements, this species should
in fact benefit from climatic warming, particularly at the
northern edge of its distribution. However, the opposite
is observed, which suggests the predominance of local
over global factors. Studies carried out to investigate this
issue have shown that several local factors explain the
decline (or even the disappearance) of local populations
of this species. Those factors include the introduction
of predators in the case of island populations (Cheylan
December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
2016), the disappearance of the European rabbit and the
resulting changes to the landscape (Grillet et al. 2010),
the impact of pest control on entomofauna prey (Doré
et al. 2015), and the abandonment of agricultural land
and the resulting progression of woodland (Grillet et al.
2006; Pottier et al. 2017). Thus, the expected effects on
reptiles of the changes caused by warming in Europe
(Araujo et al. 2006) are not borne out in the case of the
Ocellated Lizard.
Which Zones should be Surveyed in the Future to Im-
prove Our Knowledge of this Species’ Distribution?
The recent discovery of a population in Vendée (Cédric
Baudran, pers. comm. 2018), beyond the known bound-
ary on the Atlantic coast, shows that new populations
remain to be discovered, especially at the edges of the
distribution range. A priority would be to seek confirma-
tion of the true disappearance of the species in selected
sites where it was known in the past, based on the pres-
ence predictions generated by the SDMs. Secondly, an
attempt to confirm the existence of connections between
population clusters that are considered to be separated
would be interesting. This would be particularly useful
for populations located in the mountainous zones of the
Alpes-Maritimes (Deso et al. 2015), in the upper Durance
valley (Deso et al. 2011), and in the Rhdéne valley (Doré
et al. 2015), as well as the fragmented populations in the
Lozere, Aveyron, Tarn, Tarn-et-Garonne, Lot, Dordogne,
Correze, and Cantal (Geniez and Cheylan 2012; Pottier
et al. 2017). The coastal populations of the Atlantic cur-
rently seem rather well-defined (Berroneau 2012); how-
ever, this does not exclude the possibility of discovering
new populations there.
What Conservation Strategy should be Adopted to
Protect this Species?
The predictive distribution models generated in this
study provide interesting leads for defining a conserva-
tion strategy for this species. First, the current network of
protected areas in France can be considered to rather sat-
isfactorily cover the distribution range of the Ocellated
Lizard and its different population clusters. However, a
deeper analysis reveals that only a very small proportion
of the area potentially favorable to the species benefits
from strong protection regulations. The areas of land
with the strictest protection (national and regional nature
reserves, National Forest Agency ecological reserves,
and national parks) only represent 1.2% of the potential
niche of this species in France. In terms of national parks,
the Cévennes National Park clearly bears the most re-
sponsibility in terms of the conservation of this species,
followed at some distance by the Calanques National
Park (respectively, 40 and 95 km? of favorable habitats
for the species). There are 15 national nature reserves
with the presence of the species, and in this category of
Amphib. Reptile Conserv.
protected area, the reserves of Coussouls de Crau and the
Maures plain have the largest known populations (re-
spectively, 74 km? and 52 km? of favorable habitat). Of
National Forest Agency ecological reserves, 16 include
land where the lizard 1s found, with the largest being the
Maures reserve (18 km? of favorable habitat) and the Pe-
tit Luberon reserve (16 km? of favorable habitat). Some
240 Natura 2000 sites have conditions that are potentially
favorable to the species; 21 protect areas of land that con-
tribute to the conservation of the species of more than 90
km, for a total contribution of about 3,430 km? for this
category of protected area.
Given the rather dense network of protected areas,
both in terms of spatial extent and altitudinal range, a
strategy based on anticipating climate change (Salas et al.
2017) is not necessarily the best choice. As stated above,
this species is in decline at the northern edge of its dis-
tribution, which runs counter to the expected effects of a
warming climate (which is predicted for the region in the
future). Moreover, the refuge habitat for this species (and
where it originated) is located in the southern half of the
Iberian Peninsula (Miraldo et al. 2011), so the effects of
climatic warming are unlikely to be harmful to the spe-
cies at the northern edge of its distribution. In support
of this hypothesis, it has been argued that the increase
in wildfires due to climatic warming will significantly
increase the density of Ocellated Lizard populations in
the Mediterranean region, by transforming woodland
into open landscapes (Santos and Cheylan 2013). A more
important consideration than climatic warming for the
conservation of the species is that its spread relies on the
existence (or not) of favorable environments, and its de-
mographic capacity to colonize new territories. Unfor-
tunately, studies of the isolated populations at the edges
of the distribution range (Grillet et al. 2006; Deso et al.
2015; Pottier et al. 2017) show that these two parameters
are rarely present, and that these populations are, in the
more or less long term, undergoing a process of extinc-
tion (Salvidio et al. 2004; Cheylan and Grillet 2005).
From a strategic point of view, therefore, the core of
the distribution range should be prioritized for conser-
vation efforts in the long term, without neglecting cer-
tain peripheral populations in the shorter term (e.g., the
populations in the valleys of the Durance, Rhdéne, and
Var rivers, and the sandy habitats of the Atlantic coast).
Our SDM-generated maps indicate that the isolated pop-
ulations of the Atlantic coast, as well as the population
clusters west of the Massif Central (in the departments
of Aveyron, Tarn, Tarn-et-Garonne, Lot, and Dordogne),
offer climatic and topographical conditions that are very
favorable to this species. These populations, while isolat-
ed from the Mediterranean population, should be given
careful attention. They may even harbor specific genetic
compositions that warrant further consideration.
The strong dependence of the Ocellated Lizard on
the European rabbit in soft soils (Grillet et al. 2010) also
suggests the value of taking concerted conservation mea-
December 2019 | Volume 13 | Number 2 | e213
Jorcin et al.
sures that equally protect this mammal. As the demo-
graphic trends of rabbit populations in the Mediterranean
region are very negative (Ward 2005; Delibes-Mateos
et al. 2008; Poitevin et al. 2010), this could result in a
domino effect on Ocellated Lizard populations.
Conclusions
This analysis, carried out at the scale of France, reveals
that the distribution of the Ocellated Lizard is primarily
conditional on climatic factors, in particular the length of
the arid summer period. Further study at a smaller scale
would help to provide a more detailed understanding of
the ecological preferences of this species. Such a study
could consider two finer, overlapping spatial scales: the
Mediterranean coast and the region around Montpellier.
Focusing on the Mediterranean coastal plains would al-
low climatic and topographic variables to be separated
out, at least partially, to better bring to light the roles of
factors linked to land use. Including the region of Mont-
pellier would more completely isolate climatic and topo-
graphic variables, allowing a focus on habitat variables
directly linked to the ecology of the species: soil type,
crop or natural vegetation type, level of urbanization, and
the presence and density of European rabbits.
Acknowledgements.—We would like to thank all the
observers and organizations that collected the data used
in this study: the nature conservation NGOs Cistude-Na-
ture, the League for the Protection of Birds in Provence-
Alpes-Céte d’Azur (LPO PACA) and the Dréme (LPO
Dréme), Nature en Occitanie, Méridionalis, and the pub-
lic platform for naturalist data, SILENE Provence-Alpes-
Cote dAzur. We would also like to thank Elise Bradbury
for reviewing the English text.
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Laurent Barthe is responsible for biodiversity at the NGO Nature en Occitanie in Toulouse, France. Lau-
rent has been president of the French Herpetological Society since 2017. Passionate about reptiles since
childhood, he is particularly interested in snakes and the European Pond Turtle. Two of his job roles are to
broaden knowledge about reptile and amphibian distribution and promote their conservation.
Matthieu Berroneau is a herpetologist at the NGO Cistude Nature in Bordeaux, France (http://www.
cistude.org), where he specializes in the herpetofauna of southwest France, with a particular emphasis on
conservation, education, and raising awareness. A lifelong interest in amphibians and reptiles also drives
Matthieu’s work as a professional photographer (http://www.matthieu-berroneau.fr), leading him to travel
the world to take pictures of a variety of species.
Marc Cheylan is a lecturer in Conservation Biology at the Ecole Pratique des Hautes Etudes (EPHE),
an institute within the PSL Research University (Paris Sciences et Lettres). Marc joined the EPHE’s bio-
geography and ecology research laboratory after a post as the associate curator at the Natural History
Museum of Aix-en-Provence. He currently works at the French National Centre for Scientific Research
(CNRS: http://www.cefe.cnrs.fr/fr/), Centre for Functional and Evolutionary Ecology (CEFE), based at the
University of Montpellier. Author of some 200 publications and four books in the fields of ecology, bio-
geography, and the conservation of amphibians and reptiles around the Mediterranean, Marc is a member
of several nature conservation organizations, including the International Union for the Conservation of
Nature (IUCN), and also sits on various scientific advisory bodies for natural parks and reserves.
Florian Doré is a naturalist who currently works at the NGO Deux-Sevres Nature Environnement in
Deux-Seévres, western France. Florian leads monitoring surveys and conservation studies on entomofauna
and herpetofauna, and has contributed to studies of the Ocellated Lizard since 2007. He co-authored the
National Action Plan for the Ocellated Lizard in France for the NGO OBIOS (Objectifs Biodiversités)
and co-authored a monograph on the species with Pierre Grillet and Marc Cheylan that was published by
Biotope Editions. Photo by Marc Cheylan.
Philippe Geniez is a research engineer in the Vertebrate Biogeography and Ecology lab at the Ecole
Pratique des Hautes Etudes (EPHE), an institute within the PSL Research University (Paris Sciences
et Lettres). The lab is part of the French National Centre for Scientific Research (CNRS: http://www.
cefe.cnrs.fr/fr/), Centre for Functional and Evolutionary Ecology (CEFE). Author of 236 publications,
Philippe is a specialist in Western Palearctic amphibians and reptiles. His research focuses on biological
systematics, phylogeny, ecology, and the distribution of plants and animals, particularly amphibians and
reptiles.
Pierre Grillet is a naturalist who, since 1995, has been studying the Ocellated Lizard at the edge of its
distribution, particularly on the island of Oléron, the last island population of the species in France. Pierre
has written several scientific articles and co-authored two books on the Ocellated Lizard. He regularly
organizes herpetological training for the French Agency for Biodiversity. Photo by Marc Cheylan.
Amphib. Reptile Conserv. 297 December 2019 | Volume 13 | Number 2 | e213
Distribution of Timon lepidus in France
Pierre Jorcin conducts research and leads projects on biodiversity conservation, with a focus on geospatial
modelling. Pierre’s areas of interest are species distribution, ecological niche modelling, and wildlife cor-
ridor mapping. He has been involved in sustainable development programmes in South Asia for 14 years.
Pierre is currently working on flora and fauna database management for ecological ranking and environ-
mental impact assessment studies in southern France.
Benjamin Kabouche is the director of the environmental NGO LPO PACA (Ligue pour la Protection
des Oiseaux, a member of BirdLife International) in the region of Provence-Alpes-Céte d’ Azur in France
(https://paca.lpo.fr/protection). One of Benjamin’s roles is to coordinate studies and nature conservation
programs. He has contributed to several naturalist publications on the subjects of terrestrial wildlife and
biogeography.
Alexandre Movia works for the environmental NGO LPO Dréme (Ligue pour la Protection des Oiseaux),
where he is an ecological corridor specialist. Alexandre acts as an advisor on herpetology to the French
department of the Dréme, and recently conducted a study on the distribution of the Ocellated Lizard in
this region.
Babak Naimi is a researcher at the University of Helsinki, Finland, with a research focus on modelling
species distribution and biodiversity under climate change and land use change scenarios. Babak is inter-
ested in developing a quantitative understanding of ecosystem dynamics (e.g., through remote sensing and
geoinformatics tools) and uncovering the complexities behind ecosystem behavior.
Gilles Pottier has been a professional field herpetologist for some 20 years, and currently works mainly
in the Pyrenees and the Massif Central for the NGO Nature en Occitanie. A member of the French Herpe-
tological Society, Gilles runs training events in herpetology in southwest France and has written numer-
ous papers and books about the local herpetofauna, including a work on the reptiles of the Pyrenees (Les
Reptiles des Pyrénées), published in 2016 by the French Natural History Museum. Photo by J.P. Vacher.
Jean-Marc Thirion is an ecologist and the director of the NGO OBIOS (Objectifs Biodiversités) in south-
west France. Jean-Marc leads conservation projects to protect natural areas and conducts population moni-
toring of amphibians and reptiles to promote conservation initiatives. He has participated in many natural-
ist surveys of flora and fauna.
Amphib. Reptile Conserv. 298 December 2019 | Volume 13 | Number 2 | e213
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 299-303 (e214).
First field report of Trimerodytes percarinatus (Boulenger,
1899) (Reptilia: Squamata: Natricidae) from India with notes
on its natural history
1*Ashok Kumar Mallik, 2Subhadeep Chowdhury, *Bharat Bhushan Bhatt, and *Ashok Captain
‘Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560012, Karnataka, INDIA *Krishnachak, Dhurkhali, Howrah 711410, West
Bengal, INDIA *Department of Environment & Forest, P-Sector, Itanagar 791111, Arunachal Pradesh, INDIA *B-2, La Shanz Apartments, 3/1 Boat
Club Road, Pune 411001, Maharashtra, INDIA
Keywords. Arunachal Pradesh, distribution, Natricinae, new country record, Sinonatrix pericarnata, water snake
Citation: Mallik AK, Chowdhury S, Bhatt BB, Captain A. 2019. First field report of Trimerodytes percarinatus (Boulenger, 1899) (Reptilia: Squamata:
Natricidae) from India with notes on its natural history. Amphibian & Reptile Conservation 13(2) [General Section]: 299-303 (e214).
Copyright: © 2019 Mallik et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 6 November 2018; Accepted: 5 August 2019; Published: 24 December 2019
The Asian snake genus Trimerodytes Cope, 1895
belongs to the family Natricidae and consists of four
species, namely Trimerodytes annularis (Hallowell,
1856), Trimerodytes percarinatus (Boulenger, 1899),
Trimerodytes aequifasciatus (Barbour, 1908), and
Trimerodytes yunnanensis (Rao and Yang, 1998).
Trimerodytes percarinatus (Boulenger, 1899) is a
nocturnal snake commonly known as the Eastern
Water Snake or Chinese Keelback Water Snake.
This species inhabits water passages in forested hilly
country (100—2,000 m asl) and generally feeds on fish,
crayfish, crustaceans, frogs, and their larvae (Pope 1935;
Smith 1943). Pope (1935) also recorded its presence
in irrigated fields near a forest in Kuatun, China.
Currently, 7rimerodytes percarinatus has two recognized
subspecies, Trimerodytes percarinatus percarinatus
(Boulenger, 1899) and Trimerodytes percarinatus suriki
(Maki, 1931).
Trimerodytes percarinatus was originally described as
Tropidonotus percarinatus by Boulenger in 1899, from
Kuatun, Foochow, in the north-west of the Province of
Fokien (=Fujian), China at an altitude of 3,000-—4,000
ft or more (Zhao and Adler 1993). Subsequently, it was
placed within the genus Natrix by Mell (1931) and later
assigned to the genus Sinonatrix by Rossman and Eberle
(1977). Based on a recent phylogenetic study, it 1s placed
within the genus 7rimerodytes (Ren et al. 2019).
This species is distributed in north-eastern India
(Arunachal Pradesh), Myanmar, Thailand, Laos,
Vietnam, south-eastern China, and Taiwan at elevations
ranging from 90-—2,000 m (Pope 1935; Smith 1943;
Taylor 1965; Zhao and Adler 1993; Stuart and Heatwole
2008; Nguyen et al. 2009; Boundy et al. 2014). Captain
and Patel (1998) first reported the existence of the genus
Trimerodytes in India, represented by this species,
7. percarinatus, based on an uncatalogued museum
specimen housed previously at Deban Forest Camp and
now at the Namdapha Tiger Reserve Field Museum in
Miao, India. For the next two decades since then, though
studies documenting the herpetofauna of Arunachal
Pradesh have been conducted, this species has not
been recorded (Athreya et al. 1998; Borang et al. 2005;
David and Mathew 2005; Agarwal et al. 2010). Here, we
report the first field record of 7rimerodytes percarinatus
(Boulenger, 1899) from India with notes on its natural
history.
This species was recorded on two occasions in
Namdapha Tiger Reserve, Arunachal Pradesh, India.
This national park harbors a rich biodiversity and is
part of one of the world’s biodiversity hotspots (Indo-
Myanmar). The first individual (Fig. 1) was encountered
at 27°28’58”N, 96°24’ 14”E and an elevation of 515 masl,
at approximately 2200 h on 17 June 2011. It was found
inside a small ditch filled with water (~1 ft deep) near
the road edge, with its head out of the water and it was
foraging actively. The second individual was recorded at
approximately 1730 h on 18 June 2011. It was foraging
in a water passage near the edge of a road. A Fowlea cf.
piscator was also seen foraging in the same water body.
The first individual was captured for morphological
measurements and photographs, and was later released
into the wild. A detailed description of the specimen is
given in Table 1, and follows the methods from Vogel et
al. (2004). Comparisons between the left and right sides
of the head, and associated habitat where the snake was
encountered, are also presented (Figs. 2-4).
Correspondence. ':*ashokgene@gmail.com, *isuvodee mail.com, * sangobarta@gmail.com, * ashokcaptain@hotmail.com
i 8! PUES if 8! [p
Amphib. Reptile Conserv.
December 2019 | Volume 13 | Number 2 | e214
Trimerodytes percarinatus in India
Fig. 1 Full body picture of Trimerodytes percarinatus from
Namdapha, India.
Fig. 3 Habitat of Trimerodytes percarinatus at Namdapha,
India.
Morphometric data for this specimen fall within
the range of Trimerodytes percarinatus as defined
in the available literature (Pope 1935; Smith 1943).
These observations provide two additional records of
Trimerodytes percarinatus from India and the first field
report from the country, though the sightings were in
more or less the same place (“Deban’”) associated with
the earlier specimen (see Captain and Patel 1998).
This work, as well as other literature on this genus
including new range records of other congeners from
Indochina (Vogel et al. 2004; Pauwels et al. 2009; Le
et al. 2015), points out our incomplete understanding of
the distribution of this genus as a whole. Further work
is required to determine the actual distribution range of
this species in India, to understand its morphological and
genetic variation across populations, and to add to our
knowledge of its natural history.
Acknowledgements.—We would like to thank the State
Forest Department of Arunachal Pradesh for providing
permission (No. CWL/G/13(17)/06-07/PT/3838-46)
to Kartik Shanker and Ashok Kumar Mallik, Centre
for Ecological Sciences, Indian Institute of Science,
Bangalore, to carry out the fieldwork and collect samples
Amphib. Reptile Conserv.
Fig. 2 Comparison between right and left sides of the head of
Trimerodytes percarinatus from Namdapha, India.
Fig. 4 Location of first field sighting of Trimerodytes percari-
natus in Namdapha Tiger Reserve, Arunachal Pradesh, India.
in protected areas of Arunachal Pradesh. We thank
Kartik Shanker for his valuable input to our manuscript,
and for providing financial and logistic support during
our fieldwork. Also, many thanks to the Field Director,
Assistant Field Director Dr. Aporesh Gupta-Choudhury,
and other forest staff from Deban guest house, Namdapha
Tiger Reserve, for their hospitality during the fieldwork.
Literature Cited
Agarwal I, Mistry VK, Athreya RM. 2010. A preliminary
checklist of the reptiles of Eaglenest Wildlife
Sanctuary, West Kameng District, Arunachal Pradesh,
India. Russian Journal of Herpetology 17: 81-93.
Athreya RM, Captain AS, Athreya VR. 1997. A Faunal
Survey of Namdapha Tiger Reserve Arunachal
Pradesh, India: Notes on Some of the More Interesting
Species. Unpublished report. Arunachal Pradesh
Forest Department. Itanagar, Arunachal Pradesh,
India.
Borang A, Bhatt BB, Chaudhury SB, Borkotoki A, Bhutia
PT. 2005. Checklist of the snakes of Arunachal
Pradesh, northeast India. Journal of Bombay Natural
History Society 102(1): 19-26.
December 2019 | Volume 13 | Number 2 | e214
Mallik et al.
Captain A, Patel A. 1998. Sinonatrix, a new genus for
India. Hamadryad 22(2): 114-115.
Cope ED. 1895. On a collection of Batrachia and
Reptilia from the Island of Hainan. Proceedings of the
Academy of Natural Science of Philadelphia XLVI:
423-428.
David P, Mathew R. 2004. Notes on some noteworthy
snake specimens deposited in the collections of
Eastern Regional Station of the Zoological Survey
of India. Records of the Zoological Survey of India
104(3-4): 83-90.
Le DT, Pham AV, Pham CT, Nguyen SHL, Ziegler T,
Nguyen TO. 2015. Review of the genus Sinonatrix
in Vietnam with a new country record of Sinonatrix
yunnanensis Rao et Yang, 1998. Russian Journal of
Herpetology 22(2): 84-88.
Mell R. 1931. List of Chinese snakes. Lingnan Science
Journal 8: 199-219.
Nguyen VS, Ho TC, Nguyen QT. 2009. Herpetofauna of
Vietnam. Edition Chimaira, Frankfurt, Germany. 768 p.
Pauwels OSG, Kunya K, David P, Sumontha M. 2009.
First record of the Yunnan Keelback Sinonatrix
yunnanensis Rao and Yang, 1998 (Serpentes:
Natricidae) from Thailand. Salamandra 45(3): 165-
169.
Pope CH. 1935. The Reptiles of China. Pp. 116-120 In:
Natural History of Central Asia. Volume X. American
Museum of Natural History, New York, New York,
USA. 604 p.
Ren J, Wang K, Guo P, Wang Y, Nguyen TT, Li J. 2019.
On the generic taxonomy of Opisthotropis balteata
(Cope, 1895) (Squamata: Colubridae: Natricinae):
taxonomic revision of two natricine genera. Asian
Herpetological Research 10(2): 105-128.
Rossman DA, Eberle WG. 1977. Partition of the genus
Natrix, with preliminary observations on evolutionary
trends in natricine snakes. Herpetologica 1: 34-43.
Smith MA. 1943. The Fauna of British India, Ceylon, and
Burma, including the Whole of the Indo-Chinese Sub
Region. Reptilia and Amphibia, Volume 3 (Serpentes).
Taylor and Francis, London, United Kingdom. 583 p.
Stuart BL, Heatwole H. 2008. Country records of snakes
from Laos. Hamadryad 33: 97-106.
Taylor EH. 1965. The serpents of Thailand and adjacent
waters. The University of Kansas Science Bulletin
45(9): 609-1,096.
Vogel G, David P, Pauwels OSG, Brachtel N. 2004.
On the occurrence of the watersnake Sinonatrix
aequifasciata (Barbour, 1908) (Serpentes, Colubridae,
Natricinae) in Vietnam. Hamadryad 29(1): 110-114.
Wallach V, Williams KL, Boundy J. 2014. Snakes of the
World: a Catalogue of Living and Extinct Species.
Taylor and Francis/CRC Press, Boca Raton, Florida,
USA. 677 p.
Zhao E, Adler K. 1993. Herpetology of China.
Contributions to Herpetology, Volume 10. Society for
the Study of Amphibians and Reptiles in cooperation
with Chinese Society for the Study of Amphibians and
Reptiles, Oxford, Ohio, USA. 522 p.
Zhao E. 1986. Partition of Chinese Natrix species and a
suggestion of their Chinese names. Acta Herpetologica
Sinica 5(3): 239-240. [in Chinese, English summary]
Table 1. Characteristics of one specimen of 7rimerodytes percarinatus from Namdapha, Arunachal Pradesh, India, compared with
descriptions in Pope (1935) and Smith (1943).
Characters This study Pope (1935) Smith (1943)
Dorsal scale rows 19:19:17, keeled 19 19
Ventrals 153 138-143 133-157
Subcaudals 69/70 70—79 (males), 67-73 (females) 68-85
Anal Divided Divided -
vara 433 (male) 515-567 (males); 620-730 (females) 720 (male): 940 (female)
Tail length (mm) 131 130 190 (male); 270 (female)
Head length (mm) 22.1 — —
Horizontal eye 39 a =
diameter (mm)
Vertical eye diameter
3.9 w ,
(mm)
Eye to nasal distance 40 i 7
(mm)
Eye-snout distance
6.8 = -
(mm)
Inter-nasal distance 48 7 7
mm ;
Prefrontal (mm) 2.6 - —
Parietal (mm) 7.3 — —
Length of supraocular 53 _ 7
(mm)
Width of supraocular
27 a Ls
(mm)
Amphib. Reptile Conserv. 301
December 2019 | Volume 13 | Number 2 | e214
Trimerodytes percarinatus in India
Table 1 (continued). Characteristics of one specimen of 7rimerodytes percarinatus from Namdapha, Arunachal Pradesh, India,
compared with descriptions in Pope (1935) and Smith (1943).
Characters This study Pope (1935) Smith (1943)
8 (left), 4 touching eye
1 th th 1
Supralabials /9 (right), 4" and 5 9 (rarely 8 or 10), 4 and 5" entering 9, 4" and 5” touching eye
the eye
touching eye
10 (on left and right);
1‘—5" touch anterior
genials (chin shields); 5 lower labials in contact with anterior
Infralabials 5 and 6" touch chin shields that are shorter than —
posterior genials — posterior
which are longer than
anterior genials
Preoculars 1 (+1 presubocular)/ 1 single 1
3 (+1 postsubocular/ 3
Postoculars (+2 postsuboculars) 4 (occasionally 3 or 5) 7
Supraocular 1/1 - _
1 (2 fused scales) + 3/ 1 3 (occasionally 2 or 4)/ 3
Temporals (2 fused scales) + 3 (occasionally 2, rarely 4) af oeratcly Ste)
Cross bands (on 30 = ls
body)
Nostril Directed upward — Directed slightly upward
Nasal Partially divided Completely divided —
Narrowed anteriorly, Natvowed anterior: donper than Distinctly narrowed anteriorly,
Internasal longer than the usually longer than the
broad, and longer than prefrontal
prefrontal prefrontal
Prefrontal Broader than long Shorter than internasal -
; As long as broad, as long as its
Frontal Long and pointed distance from the end of snout, shorter —
posteriorly than parietals
Young: dorsum grey or dark
Dorsum greyish brown
Olive green, color descending on
with uniform cross-bars,
doisolatcrlipontion _ Dorsum greyish olive, sides with the dorsolateral side as V shaped
lichtsyellowancolor light-edged black vertical bars; venter _bars, the interval between bars
Cuibeion otter Shieh ae uniform yellowish white anteriorly, and lower portion yellowish;
iaiformaparedand spotted and speckled with blackish Adults: dorsum greyish or
anpaned Pareles posteriorly; lower surface of tails dark —_ olivaceous with uniform or with
Withtlisht yellowish grey in color along with black spots dark reticulation or dark cross-
Sane eral bars, venter whitish, with or
without dark cross-bars
Amphib. Reptile Conserv. 302 December 2019 | Volume 13 | Number 2 | e214
Amphib. Reptile Conserv.
Mallik et al.
Ashok Kumar Mallik received his Doctorate degree in 2018 from the Centre for Ecological
Sciences, Indian Institute of Science, Bangalore, India. Ashok’s research interests include
systematics, taxonomy, hybrid zones and speciation, population genomics, and evolutionary
ecology of reptiles and amphibians. He is working on the systematics and biogeography of a few
genera of colubrid and viperid snakes in Peninsular India.
Subhadeep Chowdhury received his Bachelor’s degree in Zoology from Midnapore College,
India, in 2014 and his Master’s degree in Marine Biotechnology in 2016 from the Goa University,
India. Currently, Subhadeep is working independently on the herpetofauna of West Bengal
state. His current research interests include the natural history, biogeography, and systematics of
amphibians and reptiles of India.
Bharat Bhushan Bhatt received his Doctorate degree in 2004 from the Department of Zoology,
Guwahati University, Assam, India. Bharat is presently serving as Senior Scientific Officer in the
Department of Environment and Forest at the Office of the PCCF (Wildlife and Biodiversity),
Government of Arunachal Pradesh, India. He was one of the pioneers in pursuing an interest
in the field of herpetology in the state, and in North India as a whole. Bharat has more than 30
years of field experience in various wildlife subject matters. He has contributed to 13 published
scientific papers, and compiled many survey reports, case histories, and other contributions to the
state fauna series.
Ashok Captain is a renowned Indian herpetologist who is interested in and dabbles with the
traditional taxonomy of snake species that occur in India.
303 December 2019 | Volume 13 | Number 2 | e214
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [Special Section]: 304-322 (e215).
The most frog-diverse place in Middle America, with notes
on the conservation status of eight threatened species of
amphibians
12.* José Andrés Salazar-Zuniga, '?°Wagner Chaves-Acuna, Gerardo Chaves, ‘Alejandro Acuna,
12Juan Ignacio Abarca-Odio, '*Javier Lobon-Rovira, '?7Edwin Gomez-Méndez, ‘Ana Cecilia
Gutiérrez-Vannucchi, and 7Federico Bolafos
'Veragua Foundation for Rainforest Research, Limén, COSTA RICA *Escuela de Biologia, Universidad de Costa Rica, San Pedro, 11501-2060
San José, COSTA RICA Division Herpetologia, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”-CONICET, C1405DJR, Buenos
Aires, ARGENTINA ‘*CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrario de Vairdo,
Rua Padre Armando Quintas 7, 4485-661 Vairdo, Vila do Conde, PORTUGAL
Abstract.—Regarding amphibians, Costa Rica exhibits the greatest species richness per unit area in Middle
America, with a total of 215 species reported to date. However, this number is likely an underestimate due to the
presence of many unexplored areas that are difficult to access. Between 2012 and 2017, a monitoring survey
of amphibians was conducted in the Central Caribbean of Costa Rica, on the northern edge of the Matama
mountains in the Talamanca mountain range, to study the distribution patterns and natural history of species
across this region, particularly those considered as endangered by the International Union for Conservation of
Nature. The results show the highest amphibian species richness among Middle America lowland evergreen
forests, with a notable anuran representation of 64 species. The greatest diversity in the study area occurred in
the mature forest on the basal belt. Of the 68 amphibian species found, seven (10%) are endemic to the Atlantic
versant and eight (11.6%) are threatened. This survey includes the first record of Gastrotheca cornuta in Costa
Rica since it was last reported 21 years ago. New populations of Agalychnis lemur (Critically Endangered)
and Duellmanohyla uranochroa (Endangered) are reported, and Ecnomiohyla veraguensis (Endangered) is
reported for the first time in Costa Rica. These findings show that this locality is a high priority conservation
area for a large number of amphibian species, which are often threatened by habitat loss and fragmentation.
Keywords. Biodiversity, Costa Rica, Endangered, Limon province, patterns of distribution, Tropical Wet Forest
Resumen.—En anfibios, Costa Rica exhibe la mayor riqueza de especies por unidad de area en América
Meridional con un total 215 especies documentadas a la fecha. Sin embargo, es probable que este numero este
subestimado debido a la presencia de areas inexploradas con dificil acceso. Entre 2012 y 2017, realizamos un
monitoreo de anfibios en el Caribe Central de Costa Rica, en el borde norte de la Fila Matama en la Cordillera
de Talamanca, para estudiar los patrones de distribucion y la historia natural de las especies en esta region,
particularmente aquellas consideradas en peligro por la Union Internacional para la Conservacion de la
Naturaleza (UICN). Nuestros resultados muestran la mayor riqueza de especies de anfibios en los bosques
perennes de tierras bajas de América Meridional, con una notable representacion de anuros de 64 especies.
La mayor diversidad en el area de estudio se encontro en el bosque maduro en el piso basal. Del total de
especies, siete (10%) son endemicas de la vertiente Atlantico y ocho (11,6%) estan amenazadas. Este es el
primer registro de Gastrotheca cornuta en Costa Rica después de 21 anos desde que se registro por ultima
vez. Descubrimos nuevas poblaciones de Agalychnis lemur (en Peligro Critico), Duellmanohyla uranochroa
(en Peligro), y reportamos por primera vez Ecnomiohyla veraguensis (en Peligro) en Costa Rica. Nuestros
resultados muestran que esta localidad es un area de alta prioridad para la conservacion de una gran cantidad
de especies de anfibios, a menudo amenazadas por la fragmentacion y la pérdida de habitat.
Palabras clave. Biodiversidad, Costa Rica, amenazado, provincia de Limon, patrones de distribucion, Bosque Trop1-
cal Humedo
Citation: Salazar-Zuniga JA, Chaves-Acuha W, Chaves G, Acuna A, Abarca-Odio JI, Lobon-Rovira J, Gdmez-Méndez E, Gutiérrez-Vannucchi AC,
Bolanos F. 2019. The most frog-diverse place in Middle America, with notes on the conservation status of eight threatened species of amphibians.
Amphibian & Reptile Conservation 13(2) [General Section]: 304-322 (e215).
Copyright: © 2019 Salazar-Zufiga et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 21 March 2019; Accepted: 22 December 2019; Published: 30 December 2019
Correspondence. *jsalazar@veraguarainforest.com (JASZ), wchaves512@gmail.com (WCA), cachil3@gmail.com (GC),
alejandro2 lucr@gmail.com (AA), jiao24@gmail.com (JIAO), j.lobon.rovira@hotmail.com (JLR), gedgome@gmail.com (EGM),
anagv04@gmail.com (ACGV), federico. bolanos@ucr.ac.cr (FB)
Amphib. Reptile Conserv. 304 December 2019 | Volume 13 | Number 2 | e215
Salazar-Zuniga et al.
Introduction
Currently, more than 8,000 species of amphibians have
been described worldwide, with the greatest diversity
occurring in the Neotropics (Duellman 1999a; Frost
2019), where lower Central America stands out as a
region with a substantial number of species (Campbell
1999; Duellman 2001; Savage 2002; Kubicki 2007).
However, there has been an increase in the numbers
of species designated as endangered throughout this
region since the late 1980s due to habitat deforestation
(Young et al. 2001; Stuart et al. 2004; Becker et al. 2007),
climate change (Pounds et al. 1999; Hof et al. 2011), and
infectious diseases (Lips et al. 2003; Pounds et al. 2006;
Wake and Vredenburg 2008).
Tropical forests harbor a considerable number
of amphibian species across distinct microhabitats
that are often related to water-dependent sites such
as ponds, temporary swamps, streams, tree holes,
and bromeliad axils (Duellman 1970; Savage 2002;
Lehtinen et al. 2004; Haddad and Prado 2005).
However, many other amphibians exhibit reproductive
modes that are totally independent from water bodies
(Savage 2002). For instance, frogs of the genera
Gastrotheca (Hemiphractidae), Eleutherodactylus
(Eleutherodactylidae), /ncilius (formerly Crepidophryne:
Bufonidae), Craugastor, Pristimantis, and Strabomantis
(Craugastoridae) lay encapsulated eggs out of water, in
which embryos undergo direct development and hatch
out as small adults (Savage 2002; Gray and Bland 2016).
Costa Rica is known to possess considerable
amphibian species richness per unit area (Savage 2002;
Sasa et al. 2010; Bolafios et al. 2011). However, this
great richness is likely to be underestimated due to the
presence of undiscovered and undescribed species in
areas that tend to be not easily accessible. To date, several
previous works have reported countrywide amphibian
checklists (Savage 2002; Bolafios et al. 2011; Leenders
2016). In particular, an increasing interest has focused
on documenting species occurrence and the population
status of threatened species in Costa Rica’s montane
ecosystems (Hayes et al. 1989; Abarca 2012; Acosta-
Chaves et al. 2015; Rovito et al. 2015) and tropical forests
of varying altitudinal gradients in the Pacific Slope
throughout its South (McDiarmid and Savage 2005),
Central (Laurencio and Malone 2009), and Northern
regions (Sasa and Solorzano 1995). In contrast, the
amphibian diversity of the Costa Rican Atlantic has been
broadly documented almost exclusively in its Northern
region (Donnelly and Guyer 1994; Guyer and Donnelly
2005; Whitfield et al. 2007). Only recently, Kubicki
(2008) compiled the first list of species in premontane
moist forests of the Costa Rican central-Caribbean.
Although that inventory showed the relevant diversity of
amphibians, little is known about the current population
status and distribution of amphibian species across other
areas of the mid-Caribbean.
Amphib. Reptile Conserv.
Along this region, the Talamanca mountain range
stands out as a predicted high priority conservation
area for amphibians (Garcia-Rodriguez et al. 2011).
Considering that long-term monitoring can accurately
assess population conditions (La Marca et al. 2005),
species inventories are key to covering gaps in the
distribution and natural history of endangered species in
order to determine appropriate conservation strategies
(Peloso 2010; Verdade et al. 2012). This study assessed
the local richness and species distribution of amphibians
in Veragua Rainforest Eco Research and Adventure Park
and its surroundings on the northern edge of the Matama
mountains in the Talamanca mountain range. Diversity
analysis was conducted for different types of altitudinal
belts, forests, and microhabitats found across the
sampling area, and the population status of the threatened
Species in the study area are discussed.
Materials and Methods
Study area. The study was conducted in the Central
Caribbean of Costa Rica between Las Brisas de Veragua
town (9°57°07"°N, 83°12711”E; 233 m asl) and Platano
peak (9°51’50”N, 83°14°10”E; 1,000 m asl) on the
northern edge of the Matama mountains in the Talamanca
mountain range, including Chimu peak (9°52’48’N,
83°14°13”E; 741 m asl) and Veragua Rainforest Park
(VRP; 9°55’30’N, 83°11’28”E; 420 m asl; Fig. 1). This
private reserve covers 3,200 ha of protected land ranging
from 200-420 m asl, and it comprises mature forest,
secondary vegetation at different stages of regeneration,
open areas, and dirt roads. The study site lies adjacent to
Victoria (9°55’21.73”N, 83°10’2.43”E; 410 m asl) on the
Victoria river basin and the Matama mountains. This area
is the closest point of the Talamanca mountain range to
the Caribbean Sea and it forms part of the buffer zones
of La Amistad International Park (an UNESCO World
Heritage Site), the Banano river basin protected area, and
the influence zones of the Zent, Peje, and Chirrip6 rivers,
as well as the Bajo Chirrip6 indigenous reserve (SINAC
2018). Sampling was carried out along the elevation
range 200—1,000 m asl, where two types of forest are
located according to Holdridge (1967): Basal Tropical
Wet Forest (200-600 m asl) and Premontane Tropical
Wet Forest (601—1,000 m asl). Only these altitudinal
belts are recorded and reported here, because they both
represent the Tropical Wet Forest.
Data collection. Data were collected between January
2012 and December 2017. To record the species
richness, samplings were standardized through diurnal
and nocturnal visual and acoustic recognition searches
(Crump and Scott 1994) into three transects: two in
VRP, covering approximately 4 km each (Transects A
and B), and one carried out along an 11 km trail between
the reserve and Platano peak (Transect C), including
Chimu peak halfway along the route. On each of these
December 2019 | Volume 13 | Number 2 | e215
Extreme frog diversity in Costa Rica
i on NICARAGUA
EES National Park “Barbilla”
/] National Park “La Amistad”
Indigeous Reserve “Chirripoi”
tT Indigeous Reserve “Bajo Chirripoi”
Fig. 1. Location of the study area (51 km?) in the Limon Province in the Central Caribbean area of Costa Rica. The colored points
represent the main localities of the study area: yellow (Chimt Peak), red (Platano Peak), blue (Veragua Rainforest Research and
Adventure Park), green (Las Brisas), and purple (Victoria).
transects, surveyors walked side-by-side at a constant
speed to record amphibian diversity on both sides of
the trail (Seber 1986), covering up to 10 m from each
side towards the forest. Transect A (300—420 m asl) was
located along a dirt road inside the reserve in a secondary
forest edge that included a 30 m wide natural pond and
open areas. Transect B (200-400 m asl) covered forest
trails and riparian environments within a mature forest.
Transect C (400—1,000 m asl) comprised an old wood
road (4 km) in a secondary forest and an indigenous
trail (7 km) within a pristine environment that included
natural ponds and riparian habitats along the trail.
From January 2012 to December 2012, Transect A
or B was sampled weekly during the day (6:00—11:00
h) and at night (18:00—22:00 h), totaling 27 field days
with four person hours (ph) per transect for a total search
effort of 1,728 ph. Once a year, between 2012 and 2017,
six expeditions at Transect C were conducted, totaling
13 field days of diurnal and nocturnal monitoring and a
search effort of 1,560 ph. A leaf litter plot survey (Scott
1976) was used to sample ten plots (8 x 8 m) in Chimt
peak (2014, 2017) and Platano peak (2013, 2015) on an
annual basis, for a total of 40 sampled plots.
The following information was recorded for the species
detected during monitoring: 1. Holdridge altitudinal belts:
basal (b) or premontane (p); 2. Type of forest: mature
(M) or disturbed (D; includes secondary forest and open
areas), and 3. Habitat association: riparian (R), forest (F),
or swamp (S; including temporary or permanent ponds).
If possible, one specimen per species was collected on
each Holdridge life zone. The collected specimens were
anesthetized and euthanized with lidocaine, fixed in a
10% buffered formalin solution, and later preserved in
70% ethanol solution. For all specimens, tissue samples
Amphib. Reptile Conserv.
of muscle and liver were collected and fixed in 95%
ethanol. Voucher specimens and tissue samples were
deposited at the Museo de Zoologia of the Universidad
de Costa Rica (UCR). Some specimens were collected by
third parties or other VRP researchers through occasional
encounters in random field trips.
The species list includes the information obtained from
this monitoring effort and UCR records of the Victoria
locality, covering a study area of 51 km/?, hereafter
referred to as Veragua. Additional photographic material
from collaborations with specialists in this area was
evaluated. The taxonomic nomenclature follows Frost
(2019), except for hylids in which Faivovich et al. (2018)
was followed. The conservation status of each species
was categorized according to the Red List of Threatened
Species of the International Union for Conservation of
Nature (IUCN 2019) and registered observations on the
natural history of threatened species.
Data analysis and permission. The Jaccard index (],) was
used to determine the similarity in species composition
between altitudinal belts, forest types, and habitat associa-
tion. A species accumulation curve was performed to ac-
count for species richness. Sampling was conducted under
research permit SINAC-ACLAC-PIME-VS-R-024-2016,
granted by Sistema Nacional de Areas de Conservacion
(National System of Conservation Areas, SINAC).
Results
Overall Results
The surveys recorded a total of 68 species of
amphibians, including 64 anurans distributed in 11
December 2019 | Volume 13 | Number 2 | e215
Salazar-Zuniga et al.
Number of species
2010 2011 2012 2013 2014 2015 2016 2017
Year
Fig. 2. Amphibian species accumulation curve for the 2010-
2017 period in the study area.
families and 31 genera, three salamanders of the family
Plethodontidae in two genera, and one caecilian in the
family Caeciliidae (Table 1; Plates I-V). The most
speciose families were Hylidae with 22 species (32.4%),
followed by Craugastoridae with 15 species (21.7%) and
Centrolenidae with 10 species (14.5%) [Table 1]. Six
of the 68 species (8.7%) were endemic to the Atlantic
slope of Costa Rica: Bolitoglossa alvaradoi, Oedipina
berlini, Craugastor persimilis, Diasporus amirae,
Hyalinobatrachium dianae, and Ecnomiohyla sukia. The
species accumulation curve reached an asymptotic phase
at the end of the sampling period (Fig. 2).
Low species similarity was obtained between basal
and premontane belts (i = 0.37) and the majority
of premontane species were found in the basal belt,
except for C. persimilis, D. amirae, and Pristimantis
caryophyllaceus (Table 1; Fig. 3a). Mature forests and
disturbed areas were found to share slightly more than
half of the species (I, = 0.52). A total of 19 species were
only present in mature forests, and 14 species were
detected only in disturbed areas (Table 1; Fig. 3b). The
most diverse habitats were the forest (43 sp.) and riparian
(31 sp.) environments, while 20 species were associated
with swamps (Fig. 3c; Table 1). The results show that
44 species were only found in one type of habitat; out
of these, the forest (19 sp.) was the most diverse habitat,
followed by riparian environments (16 sp.) and swamps
(9 sp.; Table 1). A medium-low similarity was found in
the composition of species between the riparian and the
forest (15 sp.; I; = 0.25), as well as between the swamps
and the forest (11 sp.; I; =0.21), although the data indicated
only a minimal similarity when comparing rivers and
swamps (2 sp.; I, = 0.04; Table 1). The only species that
were found in all three habitats were Agalychnis spurrelli
and Rhinella horribilis.
According to the IUCN conservation status, one
species is categorized as Data Deficient (DD), 54 as
Least Concern (LC), and eight in the various threatened
categories. Pristimantis altae and P. caryophyllaceus
are categorized as Near Threatened (NT); Craugastor
persimilis as Vulnerable (VU); Duellmanohyla
uranochroa, Ecnomiohyla_ veraguensis, Gastrotheca
cornuta, and Bolitoglossa alvaradoi as Endangered
Amphib. Reptile Conserv.
70
60
50
>
Number of species
es)
ro)
Basal Premontane
Altitudinal Belt
on
=)
Lv)
Number of species
Mature Disturbed
Forest Type
un
oO
Oo
Number of species
Forest
Habitat
Fig. 3. Number of species registered according to the altitudinal
belt (A), forest type (B), and habitat (C) in the study area.
Riparian Swamp
(EN); and Agalychnis lemur as Critically Endangered
(CR; Table 1). The species Hyalinobatrachium dianae,
D. amirae, C. sylviae, E. sukia, Ecnomiohyla bailarina,
and O. berlini remain uncategorized (Table 1).
Regarding the uncategorized species populations,
few populations of H. dianae were observed in isolated
streams within the basal mature forest. Populations with
several individuals of Diasporus amirae were detected
at the premontane belt. The species C. sy/viae was found
during 2011—2012 in only a few places within the forest.
Generally, the adults were observed inside tree holes
up to 3 m high. However, between 2012 and 2017, the
species was more commonly observed reproducing
throughout the year in VRP, near small artificial ponds
(length 200 cm, width 150 cm, depth 50 cm) located
within the forest. These ponds were created in 2012 by
a project of the Veragua Foundation for the Rainforest
Research “Veragua Foundation” (NGO) that aims to
establish in situ breeding sites for the conservancy and
study of the native amphibians. Ecnomiohyla bailarina
and E. sukia were detected calling from the canopy in
basal and premontane pristine forest. Oedipina berlini
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Extreme frog diversity in Costa Rica
Table 1. Checklist of amphibians of the Veragua Rainforest Eco Research and Adventure Park and its surroundings, with information
on the voucher ID (UCR), IUCN status, altitudinal belt (basal [b] / premontane [p]), forest type (mature [M] / disturbed [D]), and
habitat association (forest [F] / swamp [S] / riparian [R]).
Taxa UCR IUCNstatus Altiudinal Belts Forest Types Habitats
Aromobatidae (1)
Allobates talamancae (Cope, 1875) 21593 LC bp MD FS
Bufonidae (4)
Incilius coniferus (Cope, 1862) 21164 Le b MD FS
Incilius melanochlorus (Cope, 1877) 21983 Le bp M RF
Rhaebo haematiticus Cope, 1862 21139 Ee bp MD RF
Rhinella horribilis (Wiegmann, 1833) 21148 be b D RFS
Centrolenidae (10)
Cochranella granulosa (Taylor, 1949) 23183 Le b MD R
Espadarana prosoblepon (Boettger, 1892) Le b D R
Hyalinobatrachium chirripoi (Taylor, 1958) 21431 Le bp MD R
Hyalinobatrachium dianae Kubicki, Salazar, and 22035 b M R
Puschendorf, 2015
Hyalinobatrachium fleischmanni (Boettger, 1893) 23182 LC b MD R
Hyalinobatrachium talamancae (Taylor, 1952) 21157 LC bp M R
Hyalinobatrachium valerioi (Dunn, 1931) 21140 LG. b M R
Sachatamia albomaculata (Taylor, 1949) 21114 Le bp MD R
Teratohyla pulverata (Peters, 1873) 21153 LC b MD R
Teratohyla spinosa (Taylor, 1949) 21126 Le b MD R
Craugastoridae (15)
Craugastor brandsfordi (Cope, “1885,” 1886) 21149 LC b D F
Craugastor crassidigitus (Taylor, 1952) 21120 Le bp MD RF
Craugastor fitzingeri (Schmidt, 1857) 21150 Le bp MD F.
Craugastor gollmeri (Peters, 1863) 22550 LC bp M F
Craugastor megacephalus (Cope, 1875) ie b M E
Craugastor mimus (Taylor, 1955) 21414 Le b MD FP
Craugastor noblei (Barbour and Dunn, 1921) 21156 LC b MD F
Craugastor persimilis (Barbour, 1926) 22529 VU b M F
Craugastor polyptychus (Cope, 1886) 21121 LC bp MD F
Craugastor talamancae (Dunn, 1931) Le b D RF
Pristimantis altae (Dunn, 1942) 21145 NT bp MD RF
Pristimantis caryophyllaceus (Barbour, 1928) 21844 NT p M E
Pristimantis cerasinus (Cope, 1875) 21127 Le bp MD F
Pristimantis cruentus (Peters, 1873) 21170 Le bp M RF
Pristimantis ridens (Cope, 1866) 21096 LC bp MD RF
Dendrobatidae (4)
Dendrobates auratus (Girard, 1855) 21128 LC b MD F
Oophaga pumilio (Schmidt, 1857) 21106 Le bp MD RF
Phyllobates lugubris (Schmidt, 1857) 21143 Le b MD RF
Silverstoneia flotator (Dunn, 1931) 21986 Le bp MD RF
Eleutherodactylidae (2)
Diasporus diastema (Cope, 1875) 21415 Le bp MD RF
Diasporus amirae Arias, Chaves, Salazar, Salazar- 22010 p M F
Zufiga, and Garcia-Rodriguez, 2019
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Table 1 (continued). Checklist of amphibians of the Veragua Rainforest Eco Research and Adventure Park and its surroundings,
with information on the voucher ID (UCR), IUCN status, altitudinal belt (basal [b] / premontane [p]), forest type (mature [M] /
disturbed [D]), and habitat association (forest [F] / swamp [S] / riparian [R]).
Taxa UCR IUCN status Altiudinal Belts Forest Types Habitats
Hemiphractidae (1)
Gastrotheca cornuta (Boulenger, 1898) 21017 EN bp M R
Hylidae (23)
Agalychnis callidryas (Cope, 1862) 21098 1, & bp MD FS
Agalychnis lemur (Boulenger, 1882) 21104 CR bp MD S
Agalychnis saltator Taylor, 1955 21429 1 @ b MD FS
Agalychnis spurrelli (Boulenger, 1913) 21119 Le b MD RFS
Boana rufitela (Fouquette, 1961) Le b M S
Cruziohyla sylviae Gray, 2018 21422 b MD FS
Dendropsophus ebraccatus (Cope, 1886) 21103 Le b MD
Dendropsophus phlebodes (Stejneger, 1906) 21432 | D
Duellmanohyla rufioculis (Taylor, 1952) Le bp M R
Duellmanohyla uranochroa (Cope, 1875) 22002 EN bp M RF
Ecnomiohyla bailarina Batista, Hertz, Mebert, 22287 b M F
Kohler, Lotzkat, Ponce, and Vesely, 2014
Ecnomiohyla sukia Savage and Kubicki, 2010 22940 bp M
Ecnomiohyla veraguensis Batista, Hertz, Mebert, 21941 EN bp
Kohler, Lotzkat, Ponce, and Vesely, 2014
Hyloscirtus palmeri (Boulenger, 1908) 21995 LG b MD R
Isthmohyla lancasteri (Barbour, 1928) 21994 LC b M R
Scinax boulengeri (Cope, 1887) Le b D S
Scinax elaeochroa (Cope, 1875) 21151 LC b D FS
Smilisca manisorum (Taylor, 1954) Le b D S
Smilisca phaeota (Cope, 1862) 21113 Le b MD S
Smilisca puma (Cope, 1885) LC b D S
Smilisca sordida (Peters, 1863) 21099 Le b MD R
Tlalocohyla loquax (Gaige and Stuart, 1934) 21097 Le b MD S
Leptodactylidae (2)
Leptodactylus melanonotus (Hallowell, 1861) 21518 Le b D FS
Leptodactylus savagei Heyer, 2005 20107 Le b MD FS
Microhylidae (1)
Hypopachus pictiventris (Cope, 1886) Le b D SF
Ranidae (2)
Lithobates vaillanti (Brocchi, 1877) 21101 LC b D R
Lithobates warszewitschii (Schmidt, 1857) 21102 LE b MD RF
Plethodontidae (3)
Bolitoglossa alvaradoi Taylor, 1952 22048 EN b M
Bolitoglossa colonnea (Dunn, 1924) 21178 LE bp MD
Oedipina berlini Kubicki, 2016 22882 b D F
Caeciliidae (1)
Caecilia volcani Taylor, 1969 DD b D F
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Extreme frog diversity in Costa Rica
ie ee VE
Plate I. Photos in life o
bag
aie
f amphibians recorded in the sampling area: (A) A//obates talamancae; (B) Incilius coniferus, (C) I.
melanochlorus, (D) Rhaebo haematiticus, (E) Rhinella horribilis, (F) Cochranella granulosa, (G) Espadarana prosoblepon, (H)
Hyalinobatrachium chirripoi; (1) H. dianae; (J) H. fleischmanni, (IX) H. talamancae; (L) H. valerioi; (M) Sachatamia albomaculata;
(N) Teratohyla pulverata, and (O) T: spinosa. Photos by Victor Acosta-Chaves (C, G, N); Javier Lobon-Rovira (A, F, L, M, O); José
Andrés Salazar-Zuniga (B, D, E, H, J, K); Andréi Solis (1).
was observed once in the secondary basal forest, as an
individual was on the leaf litter on one of the trails of the
Veragua Rainforest Park at night.
Observations on the Threatened Species
Pristimantis altae (NT; Plate II-K) was seen and heard in
mature and secondary forests (Table 1). At the basal belt,
Amphib. Reptile Conserv.
isolated males were recorded on riversides and inside
the forest; nevertheless, at the premontane belt, groups
of at least six calling males were registered, found very
close to each other (2-3 m apart). At the premontane
belt, P. caryophyllaceus (NT; Plate H-L) was commonly
observed perched on leaves in the understory (100-150
cm high). On one occasion, a female was found in
brooding position over a fully developed clutch with 26
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Salazar-Zuniga et al.
Plate II. Photos in life of amphibians recorded in the sampling area: (A) Craugastor brandsfordi; (B) C. crassidigitus, (C)
C. fitzingeri, (D) C. gollmeri;, (E) C. megacephalus, (F) C. mimus; (G) C. noblei; (H) C. persimilis; (I) C. polyptychus, (J) C.
talamancae, (KK) Pristimantis altae, (L) P. caryophyllaceus, (M) P. cerasinus; (N) P. cruentus, (O) P. ridens. Photos by Victor
Acosta-Chaves (C, F); Javier Lobon-Rovira (B, K, O); José Andrés Salazar-Zurtiga (A, D, E, G-J, L—-N).
eggs inside a partially rolled leaf at 1 m high. The female
and her eggs were collected and placed in a plastic bag,
and the next day all the eggs had hatched inside the bag.
Craugastor persimilis (VU; Plate II-H) was observed
several times during the plot survey, hidden in the leaf
litter in the premontane belt.
Duellmanohyla uranochroa (EN; Plate IV-E) was
detected in a few streams in pristine forest (Table
1). Males were observed calling from the streamside
Amphib. Reptile Conserv.
vegetation. Also, a male chorus was heard inside the forest
at a distance of at least 100 m from the nearest stream.
Some of these individuals were located in between the
aerial roots of a walking palm (Socratea exorrhiza).
Ecnomiohyla veraguensis (EN; Plate 1V-H) was observed
once calling from the canopy in the basal mature forest.
Gastrotheca cornuta (EN; Plate III-G) was uncommon in
the survey samplings. Only two populations are known
in the study area; one of them was last reported in 1996
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Extreme frog diversity in Costa Rica
| \ By, ha . ee 5 }
Plate III. Photos in life of amphibians recorded in the sampling area (unless otherwise specified, all photographs refer to specimens
detected in Veragua): (A) Dendrobates auratus, (B) Oophaga pumilio, (C) Phyllobates lugubris, (D) Silverstoneia flotator, (E)
Diasporus diastema, (F) Diasporus amirae; (G) Gastrotheca cornuta (Veraguas, Panama); (H) Agalychnis callidryas, (1) A. lemur;
(J) A. saltator;, (IK) A. spurrelli, (L) Boana rufitela. Photos by Abel Batista (G); Javier Lobon-Rovira (A-C, E, H, I, K, L); José
Andrés Salazar-Zutiga (D, F, J).
at 200 m asl in the Victoria river basin (Solorzano et al.
1998), and the subsequent record was published 16 years
later, in the streamside vegetation in a deep canyon of the
Zent River at 550 m asl (Salazar 2015).
Three populations of the Critically Endangered
Agalychnis lemur (Plate III-[1) were observed throughout
Veragua. One of the populations was located in a pond
(width 35 m) in a mature premontane forest, where
many males were observed calling from the vegetation
at 50-150 cm high. The other two populations were
found in secondary forest at the basal belt, including a
population that is on the border of the VRP (Table 1).
Outside the reserve, this species was observed in small
ponds and flooding banks next to a wood extraction
road. Thus, given this immediate threat, small artificial
ponds (length 200 cm, width 150 cm, depth 50 cm)
were created by the Veragua Foundation during 2015
Amphib. Reptile Conserv.
to protect this population. As of 2016, it was easier to
observe individuals throughout the year during high-
humidity nights near these reproductive sites.
Discussion
With 215 species, Costa Rica is the 19™ richest country
in the world for amphibians, and exhibits the highest
richness per unit area in Middle America (Kubicki 2008;
Frost 2019). In this region, amphibian species density
seems to be greater towards the South, specifically in
Costa Rica and Panama (Campbell 1999). The results
presented here show that Veragua exhibits the highest
known species richness among Middle American lowland
evergreen forests. With a notable anuran representation of
64 species in 51 km? surveyed (Table 1; Plates I-V), these
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Salazar-Zuniga et al.
Plate IV. Photos in life of amphibians recorded in the sampling area (unless otherwise specified, all photographs refer to specimens
detected in Veragua): (A) Cruziohyla sylviae; (B) Dendropsophus ebraccatus, (C) D. phlebodes; (D) Duellmanohyla rufioculis; (E)
D. uranochroa,; (F) Ecnomiohyla bailarina (Darien, Panama); (G) E. sukia; (H) E. veraguensis (Veraguas, Panama); (1) Hy/oscirtus
palmeri; (J) Isthmohyla lancasteri;, (KK) Scinax boulengeri;, (L) S. elaeochroa, (M) Smilisca manisorum, (N) S. phaeota; (O) S.
puma, (P) S. sordida; (Q) Tlalocohyla loquax. Photos by Victor Acosta-Chaves (M); Abel Batista (F), Edwin Gomez-Méndez (O);
Daniel Hernandez (C); Andreas Hertz (H); Javier Lob6n-Rovira (A, B, J, N); José Andrés Salazar-Zutiga (D, E, G, I, K, L, P, Q).
Amphib. Reptile Conserv. 313 December 2019 | Volume 13 | Number 2 | e215
Extreme frog diversity in Costa Rica
Plate V. Photos in life of amphibians recorded in
ald -
i
melanonotus: (B) ib. savagei: (C) Hypopachus
pictiventris; (D) Lithobates vaillanti;, (E) L. warszewitschii; (F) Bolitoglossa alvaradoi, (G) B. colonnea, (H) Oedipina berlini; (1)
Caecilia volcani. Photos by Victor Acosta-Chaves (C, D, F); Esmeralda Arévalo (1); Javier Lobon-Rovira (E); José Andrés Salazar-
Zuniga (A, B, G, H).
surveys reveal one of the highest numbers of amphibian
species reported per unit area in the Neotropics (Savage
2002; Boza-Oviedo et al. 2012; Barrio-Amoros et al.
2011; Hertz et al. 2012; Arias and Bolafios 2014; Ferreira
et al. 2017).
In comparison with the most important diversity
hot spots from South America, the richest region of
amphibian species worldwide (Ron et al. 2018; Frost
2019), Veragua is also one of the most diverse localities
in the Neotropics with 68 species. Only certain sites
across the Amazon lowlands exhibit a greater richness
of amphibians than these Veragua sites (Barrio-Amor0os
et al. 2011; Ferreira et al. 2017). For example, amphibian
richness in Brazil ranged from 18 species (Alter do Chao,
Para) to as many as 78 species along a small section of
the Jurua river (Zimmermann and Rodrigues 1990; Lima
2008; Queiroz et al. 2011; Pereira-Junior et al. 2013;
Araujo and Costa-Campos 2014; Alves-Binicio and
Dias-Lima 2017; Ferreira et al. 2017; Lima et al. 2017),
with the extreme exception of 109 amphibian species in
the middle of the Xingu River (Vaz-Silvia et al. 2015;
Ferreira et al. 2017). In Peru, the most diverse sites are
in Bajo Rio Llullapichis (74 sp.; Schluter et al. 2004),
Parque Nacional Manu (68 sp.; Morales and Mcdiarmid
1996), and Cuzco Amazonico (64 sp.; Duellman 2005;
Barrio-Amoros et al. 2011). In Colombia, the highest
diversity was found in Leticia 97 species (Lynch 2005),
Amphib. Reptile Conserv.
and the two most important inventories reported in
Ecuador are from the village of Santa Cecilia (87 sp.;
Duellman 1978) and Parque Nacional Yasuni (135 sp.),
currently the most diverse amphibian site in the world
(Ron et al. 2018).
In Costa Rica, the amphibian richness is concentrated
in the southern lowlands of the country and in the
northeastern Atlantic versant (Campbell 1999;
McDiarmid and Savage 2005; Santos-Barrera et al.
2008). Compared to the three other major inventories
in these areas, Veragua is more species-rich than either
the South Pacific locality of Rincon (47 sp., Anura [42]/
Caudata [4]/Gymnophiona [1]; McDiarmid and Savage
2005), the Atlantic versant sites of La Selva Biological
Station (52 sp., 47/3/1; Guyer and Donnelly 2005),
or Guayacan (66 sp., 58/6/2; Kubicki 2008). Other
important inventories were reported in a transitional wet-
dry forest in the locality of Carara (39 sp.; Laurencio and
Malone 2009), and among the richest sites in dry forests
is Finca Taboba, at the northern edge of the country (21
sp.; Campbell 1999).
The low diversity of salamanders found in Veragua
could be due to fact that the sampling area was below
1,100 m asl, and that only one monitoring was conducted
per year in the premontane belt. It is also possible that
the sampling method was not inclusive enough to cover a
broader diversity in the basal belt. The number of frog and
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Salazar-Zuniga et al.
salamander species distributed along specific elevations
in Middle America follows a pattern previously noted in
Guatemala and Belize, 1.e., a moderate number of species
in the lowlands that progressively increases as it reaches
moderate or intermediate elevations, and then declines
precipitously at higher elevations (Campbell and Vannini
1989; Wells 2007). Salamanders partly show this pattern
as they exhibit a more dramatic increase in species in the
highlands (Campbell 1999; Wells 2007). We presume
that some other species, such as Bolitoglossa striatula,
Nototriton matama, Oedipina carablanca, and Oedipina
gracilis, which occur in the Atlantic Versant at a similar
altitudinal belt and close to the Talamanca mountain range
(Savage 2002; Kubicki 2008; Leenders 2016), could
also occur in Veragua. Among caecilids, only Caecilia
volcani was found. The apparent low diversity in this
group is probably caused by its fossorial habits (Peloso
2010; Ferreira et al. 2017) which undermine effective
sampling. We think that at least one common caecilid
species in the Atlantic Versant (Gymnophis multiplicate)
could be present in Veragua (Leenders 2016).
In this study, the basal belt was found to be more
diverse than the premontane (Fig. 3; Table 1). This is a
generalized pattern of distribution among anurans (Savage
2002) and should account for the vast representation of
frogs and toads in this study, which represent 94% of the
total amphibian species. The latter species distribution is
similar to that of the wet slopes of the Andes, the region
with the highest diversity of anuran species in the world
(Duellman 1999b; Wells 2007). The higher number
of anuran species in old mature forests compared with
disturbed areas might be explained by the presence of
more microhabitats in pristine environments (Table 1;
Savage 2002; Acosta-Chaves et al. 2015). Nevertheless,
one of the main factors shown to influence high local
and regional diversity is the variety of habitats with
numerous vegetation types, ranging from forests to open
grasslands, that occur side-by-side in the landscape, each
of them harboring a different array of species (Colli et al.
2002; Nogueira et al. 2009; Lopes-Santos et al. 2014).
The greatest species diversity and the highest level
of endemism for amphibians in Middle America occur
along the windward mesic slopes of major mountain
ranges between elevations of 800 and 2,800 m asl,
which in Costa Rica include the Guanacaste, Tilaran,
and Talamanca mountain ranges (Campbell 1999). The
Talamanca mountain range is recognized as a site of
speciation and a dispersion center for several species with
a high degree of endemism (Arias and Bolafios 2014).
Among amphibians and reptiles, 27% of the species in
Costa Rica are endemic to this region (Campbell 1999;
Savage 2002; Chaves et al. 2009; Streicher et al. 2009;
Boza-Oviedo et al. 2012; Arias and Bolafios 2014). In
this study, 8.7% of the amphibians are endemic to the
Atlantic Versant of Costa Rica (Campbell 1999; Leenders
2016; Frost 2019), including species of the genera
Duellmanohyla and Isthmohyla, which are endemic to
Amphib. Reptile Conserv.
Middle America (Faivovich et al. 2018).
A high number of species was found along the forest
and the riparian habitats (Fig. 3; Table 1). This association
with a type of forest might be due to the great variety of
microhabitats found throughout these environments that
result from irregular topography (Wells 2007; Kubicki
2008). Leaf litter is an important habitat for anurans,
especially among species with terrestrial reproduction
(although it is not restricted to them; Wells 2007). The
high moisture levels found in the forest floor allow
terrestrial species to forage and call during either the day
or night (Wells 2007). The species richness of leaf litter
frogs and toads is positively correlated with the number
of wet months and the litter mass depth (Wells 2007;
Whitfield et al. 2007).
The distribution along the riparian habitats was found
to be non-uniform, as it could rely on vegetation coverage
and the physical characteristics of the environment. The
high number of amphibian species found along riparian
habitats in this study could be due to the numerous springs,
streams, and torrents found throughout the sampling area
(Fig. 1), which generate several microhabitats along this
environment (McDiarmid and Savage 2005; Kubicki
2007; SINAC 2018). Previous studies found a similar
distribution pattern in Guayacan, where 35% of the
Species are associated with lotic environments (Kubicki
2008), while glass frogs represent more than 16% of the
amphibian diversity in La Selva (Guyer and Donnelly
2005) and Rincon (McDiarmid and Savage 2005). In the
mountainous regions of Middle America, the permanent
or temporary ponds required for amphibian breeding
are often scarce (Wells 2007). This pattern is also seen
at Veragua and Guayacan, where the highly irregular
topography of these localities causes permanent ponds
to be a much more limited resource for reproduction
(Kubicki 2008). Nevertheless, pond-breeders account
for a notable representation of anuran species in Veragua
(32, 4%) and Guayacan (30%; Kubicki 2008).
The species accumulation curve reached an asymptote,
meaning that the sampling effort to detect species
produced a number near the maximum expected value
(Fig. 2). Nevertheless, there may be some cryptic species
groups with high variation, and this fact may obscure the
estimates given here, as different species could be hidden
under a single name (Funk et al. 2012; Alves-Binicio
and Dias-Lima 2017). However, the clarification of such
unknown diversity requires further integrative taxonomic
studies. Likewise, we suggest a larger survey effort in the
premontane belt, since the difficult access to sampling
areas did not allow for a continuous sampling.
Comments on Threatened Species
This study registered P altae (NT), which has been
previously reported in very few places on the Atlantic
Slope of Costa Rica and northwestern Panama (Leenders
2016). Overall, there is only limited information about
December 2019 | Volume 13 | Number 2 | e215
Extreme frog diversity in Costa Rica
its natural history, population trends, and conservation
needs (Leenders 2016). Historically, P. altae has been
associated with undisturbed areas (Savage 2002; Pounds
et al. 2008a). Even though this species was observed in
mature forests, it was also commonly detected close to
streams within secondary forests. According to Savage
(2002), this species is mute; however, during high
humidity dark nights it is common to hear the species
emitting a short two note call “clock-clock,” similar
to the sound that two glass marbles emit when they hit
each other twice very rapidly. In basal secondary forests,
isolated males were heard calling in the forest. However,
on the premontane belt, this species is more abundant,
and several males were heard calling at a close distance
from each other. Unfortunately, the calls are emitted
sporadically, and have not yet been recorded.
In this study, P. caryophyllaceus (NT) was one of
the most common frogs in the mature premontane belt.
During the mid-1980s, when many populations in Costa
Rica declined (Leenders 2016), P. caryophyllaceus
disappeared from most lowlands; however, it persisted
at higher elevations (Leenders 2016). This pattern is
rare among Neotropical anurans, considering that more
pronounced declines generally occur at mid- and high
elevations; in Panama, populations declined dramatically
in some highlands, but in Costa Rica they seem to be
recovering in areas above 800 masl (Savage 2002; Pounds
et al. 2008b; Leenders 2016). A female was found inside
a rolled leaf at 100 cm above the forest floor attending
a mass of 29 eggs. This same behavior was previously
reported in Panamanian populations by Myers (1969).
Recent research showed that Craugastor persimilis (VU)
is susceptible to habitat fragmentation and it is often
absent in open pasture lands and pineapple plantations
(Bolafios et al. 2008). This observation 1s consistent with
the observations reported here, as this species was only
observed in the mature premontane forest.
Duellmanohyla uranochroa (EN) was a historically
common species across humid lowland and mountain
forests (Savage 2002). However, it has declined
precipitously since the late 1980s. By 2002, D. uranochroa
had experienced a significant decline across several
populations in Costa Rica (Duellman 2001; Savage 2002;
Leenders 2016; IUCN 2019). However, since 2007 some
populations have reappeared in Monteverde, the Matama
mountains, and Tuis de Turrialba (NatureServe and IUCN
2013), as well as in western Panama (Hertz et al. 2012).
In this monitoring effort, populations were observed
at the premontane and basal belt of the mature forest,
sometimes close to riparian environments. Generally,
males were found on the forest floor or on walking palm
roots, and up to 2 m high. Similar behaviors have been
reported in other populations of this species (Duellman
2001; Savage 2002; NatureServe and IUCN 2013).
Before this report, Ecnomiohyla veraguensis was
only known from two small Panamanian populations in
Santa Fé National Park, where it 1s highly threatened by
Amphib. Reptile Conserv.
ongoing habitat modification due to forest clearance for
agriculture and open pit mining (IUCN SSC Amphibian
Specialist Group 2019). Ecnomiohyla veraguensis 1s
differentiated here from £. miliaria, another congener
from the Caribbean foothills, based on the presence of
scalloped fleshy fringes and the absence of heel tubercles
in the former (Batista et al. 2014); from E. bailarina,
considering that E. veraguensis has a finely tuberculate
dorsum (strongly tuberculate in EF. bailarina) with
scattered minute keratin tipped tubercles on the posterior
part of the body and 6—8 widely spaced, keratinized black
spines bordering the outer side of the thumb (two clusters
of numerous, small nuptial spines in EF. bailarina; Batista
et al. 2014). The most similar species to E. veraguensis is
E. sukia,; however, the latter lacks nuptial spines in adult
males (Batista et al. 2014).
Gastrotheca cornuta (EN) is considered a rare species
in Colombia and Costa Rica, while it has declined in
Ecuador and Panama (Coloma et al. 2008; AmphibiaWeb
2009). In Costa Rica, this species is known from only
three localities in the Limon Province (Coloma et al.
2008). The first specimen was collected during 1984 in
the northwest of Nimaso peak in the Talamanca Mountain
range at 700 m asl (Solorzano et al. 1998; Savage 2002).
The other two localities were reported in Veragua, also
at basal mature forests (Solorzano et al. 1998; Salazar
2015).
Bolitoglossa alvaradoi (EN) was only observed once
in the mature forest. This endemic species has only
been reported in undisturbed areas and it is considered
endangered because its extent of occurrence is less than
5,000 km? (Bolafios et al. 2008). This salamander is a
rare species, mostly due to its secretive arboreal habitats
(Bolafios et al. 2008). In the current survey, this species
was found during the day near a small stream on a leaf at
100 cm. Some other studies reported individuals inside
bromeliads and leaf axils during the day (Wake 1987;
Savage 2002).
Agalychnis lemur (CR) occurs in Costa Rica, Panama,
and marginally in Colombia (Solis et al. 2008). It inhabits
basal and premontane humid forests and has been
historically associated with pristine areas (Duellman
2001; Savage 2002). This species has always been fairly
uncommon throughout its range; however, it was listed
as Critically Endangered because of ongoing drastic
population declines, estimated to be more than 80% over
a ten-year period (Solis et al. 2008). This survey found
three separate natural breeding populations in the study
area. One of these populations was already reported in
Costa Rica and was considered the only remnant wild
breeding population (Solis et al. 2008). Another small
population was reported in Guayacan (Kubicki 2008;
Solis et al. 2008). All other previously known Costa
Rican populations of this species have disappeared,
including those in Monteverde, San Ramon, Braulio
Carrillo, and Tapanti (Solis et al. 2008).
The main threats reported for A. /emur are habitat
December 2019 | Volume 13 | Number 2 | e215
Salazar-Zuniga et al.
destruction and chytridiomycosis (Solis et al. 2008). In
one of the reported populations in this study, Whitfield
et al. (2017) found a low infection prevalence (<10%,
n = 20) of Batrachochytrium dendrobatidis (Bd) and
a low infection intensity among infected individuals.
Some studies demonstrated that highly Bd-susceptible
amphibians persist in environments hostile to Bd, even
when &d 1s still present (Puschendorf et al. 2011). The
samplings reported here never registered a sick animal.
Nonetheless, in some places where it was common to see
the species during the sampling surveys, A. /emur had
disappeared after the intensification of wood extraction
during 2013. Agalychnis lemur appears to be highly
susceptible to habitat loss, and the lack of natural
reproductive sites in the forest promotes the use of the
flooding banks or small ponds at the forest edge (JASZ,
pers. obs.), a condition that we consider makes this
species extremely vulnerable to habitat fragmentation.
This study shows that the threatened species reported
here are associated with mature forest. These species
may be sensitive to changes in their environment and
might therefore exhibit a low tolerance to human impact
(Dixo and Martins 2008; Lopes-Santos et al. 2018). The
main biodiversity threats observed while conducting
this study were: 1. Habitat destruction (legal or illegal)
due to population growth, pastures, and extraction
labors for wood and stone; 2. Monocultures of extensive
plantations (e.g., by banana and pineapple corporations
in the nearby lowlands), that also create substantial soil
erosion and use numerous agrochemicals to maintain
the crops, producing substantial amounts of pollution
residues (Castillo et al. 1997; Castillo and Ruepert 2001;
Sasa et al. 2010); 3. Illegal wildlife extraction; 4. Little
control by the responsible authorities; and 5. Low levels
of environmental education.
Conclusions
This survey shows that Veragua is a high priority
conservation area with 11.7% of its amphibian diversity
under the IUCN threatened categories, out of which
five species are cataloged as Endangered or Critically
Endangered (Table 1; IUCN 2019). In addition, this
study reports E. veraguensis in Costa Rica for the first
time and represents the only locality known for E.
bailarina (Kubicki and Salazar 2015). The diversity
analysis reveals one of the most important amphibian hot
spots in the Neotropics, with evidence of recent sightings
of several species after concerning declines (like those
of Duellmanohyla uranochroa and Agalychnis lemur),
and contrasts with the decimated diversity in several
other important locations in Costa Rica (e.g., La Selva,
Rincon de Osa, Cerro Chompipe, Monteverde, Cerro de
la Muerte, Tapanti, Volcan Cacao, Palmar Norte, and Las
Tablas) that have declined or disappeared since the late
1980s (Whitfield et al. 2007; Sasa et al. 2010; Ryan et al.
2015). Based on these findings, we suggest a long-term
Amphib. Reptile Conserv.
monitoring of the biodiversity in order to have control
over population fluctuations, and we highly recommend
natural history and behavioral studies to improve
conservation actions across this biodiversity hot spot.
According to the international conservation agreements,
as well as Costa Rica’s laws and executive decrees, the
information provided in this article should help to protect
the area from invasive activities that may negatively
affect the biodiversity or major river basins (Sasa et al.
2010).
Acknowledgements.—This research was possible thanks
to the invaluable help of the following group of researchers
and field assistants: José Brenes-Andrade, Andrés Royas-
Valle, Erick Arias, Diana Salazar, Iria Chacon, Victor
Acosta-Chaves, Adrian Garcia-Rodriguez, Marcelo
Elizondo, Rolando Ramirez, Julissa Gutiérrez-Figueroa,
Irene Ossenbach, Alejandro Quesada-Murillo, Melissa
Diaz-Morales, and Diego Salas. For photographic
material, we are thankful for the collaboration of Victor
Acosta-Chaves, Esmeralda Arévalo-Huezo, Abel Batista,
Daniel Hernandez, Andreas Hertz, and Andréi Solis. We
also appreciate the help of Tim Bray and Cesar Barrios-
Amoros as external reviewers, and Steve McCormack
and Cindy Chaves as English reviewers. It is important
to highlight the participation of Luis Angel Mejia
Gonzales (Pecas), Stanley Salazar, and Julian Solano
Salazar for their great efforts in searching for and finding
the species Gastrotheca cornuta and the three species
of Ecnomiohyla; to Johnny Hernandez and the sisters
Mariana and Isabella Jiménez for finding the species
Oedipina berlini, and to Esmeralda Arévalo-Huezo
and the zoology class (2018) of the Universidad Latina
(Costa Rica) for finding the only caecilid in the survey
(C. volcani). We are very grateful for the participation
of the local people of the communities of Las Brisas,
El Peje, and the Cabecar Ethnic Group, especially to
the indigenous leader Ruperto Lopez Camacho, who
shared his knowledge and guided us into the pristine
forest. We appreciate the logistic support provided by
the School of Biology and the Museum of Zoology of
the University of Costa Rica, as well as the great help
from the employees of Veragua Rainforest Research and
Adventure Park to conduct this project. Finally, we thank
The Veragua Foundation for the Rainforest Research and
its president, José Marti Jiménez-Figueres, for financing,
believing, and supporting this important research for the
conservancy.
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José Andrés Salazar-Zufiiga is a biologist and M.Sc. student in the Department of Ecology at
Universidad Autonoma de Madrid and Universidad Complutense de Madrid, Spain. He is a
professor of herpetology and an active researcher of the Herpetology Department of the University
of Costa Rica, and research coordinator of the Veragua Foundation, Limon, Costa Rica (NGO).
José’s research interests include animal behavior, natural history, and conservation of amphibians
and reptiles. He has participated in several conservation workshops organized by the Amphibian
ti
a > Specialist Group and the University of Costa Rica, including the workshops to review the IUCN
a *% . | | ii \
Red List of amphibians of Costa Rica and for elaborating the amphibian conservation strategy for
Mesoamerica. José is an active conservationist who participates in different environmental education
programs in rural communities, and he is currently developing different research and conservation
projects with various species of the Centrolenidae, Dendrobatidae, and Hylidae families.
Wagner Chaves-Acufia is a Ph.D. student in the Department of Biodiversity and Experimental
Biology at Universidad de Buenos Aires, Argentina, and a fellow of Consejo Nacional de
Investigaciones Cientificas y Técnicas (CONICET) at the Museo Argentino de Ciencias Naturales
“Bernardino Rivadavia,’” Argentina (MACN). Wagner is also an associated researcher at Veragua
Foundation, where he has conducted research on bioacoustics and behavior of dendrobatids and
centrolenids. His current research interests include systematics, taxonomy, and evolution of hylids,
as well as conservation projects with critically endangered species of anurans.
Gerardo Chaves is a biologist from the University of Costa Rica. Gerardo’s degree thesis focused
on the arrivals of the Olive Ridley Sea Turtles, but most of his professional work has focused on
the ecology and taxonomy of the Costa Rican herpetofauna. Since 1992, his research activity has
focused on understanding the decline of amphibian populations in Mesoamerica and on filling the
herpetofauna inventory gaps in several areas of Costa Rica, mainly across the Talamanca Mountain
Range. Since 1997, Gerardo has worked in the Museum of Zoology of the University of Costa Rica
in the herpetofauna collection. He has published several journal articles related to the ecology and
taxonomy of Neotropical herpetofauna. His conservation efforts are related to the sustainable use of
the sea turtle eggs project on “arribadas” and collaboration with IUCN in the evaluation of the Red
List for Costa Rica and Mesoamerica, for both reptiles and amphibians. Gerardo is currently chair
of the IUCN Amphibian Specialist Group in Costa Rica.
Amphib. Reptile Conserv. 224 December 2019 | Volume 13 | Number 2 | e215
Amphib. Reptile Conserv.
Extreme frog diversity in Costa Rica
Alejandro Acufia is a professional in Ecotourism Management, and he has worked as a coordinator
of biodiversity projects in several national parks with the National System of Conservancy Areas
(SINAC). Alejandro is a naturalist guide at Veragua Rainforest and research assistant of the Veragua
Foundation.
Juan Ignacio Abarca-Odio is a biologist from the University of Costa Rica, where he collaborates
as a researcher in the Aquatic Experimentation Laboratory (CIMAR) and the Laboratory for
Experimental and Comparative Pathology (LAPECOM). Juan’s main interests are on the effects
of climate change on the ecology and physiology of vulnerable organisms such as anthozoans,
arthropods, amphibians, and reptiles. He also has great interest in data science.
Javier Lobon-Rovira is a Wildlife Photographer and a Ph.D. student at the CIBIO-InBio institution
in Portugal. Javier has assisted as an Animal Care Volunteer at Wildlife Rescue Association
(Vancouver, British Columbia, Canada) rehabilitating wildlife and promoting the welfare of wild
animals in the urban environment. He has worked as a field assistant with Moose and Wolves in
Utah, and sampling fishes using electric-fishing techniques. For his Master's thesis, Javier identified
a “lost population” of Iberian Lynx by anecdotal occurrence data and molecular scatology, which
formed a major part of his M.Sc. degree. Furthermore, he has collaborated on many different
herpetology and conservation projects. Currently, his Ph.D. project focuses on the systematics and
evolution of geckonids from Southern Africa, which includes the descriptions of species and the
identification of several evolutionary hypotheses within this group.
Edwin Gémez-Méndez is biologist from the University of Costa Rica. Edwin has work as an
Environmental Manager in several important national projects, such as the Reventazon Hydroelectric
Project, expansion of the National Route 32, and the Costa Rica-Panama Binational Bridge. Edwin
is a Biology professor at Florencio del Castillo University, Costa Rica. His research interests concern
the conservation of amphibians and reptiles.
Ana Cecilia Gutiérrez-Vannucchi is a biologist and M.Sc. student at the School of Biology of
the University of Costa Rica, where she is part of the Laboratory of Urban Ecology and Animal
Communication (LEUCA). Ana’s research interests are in ecology, bioacoustics, and animal
behavior. Her most recent projects have focused on studying the possible effects of urban noise on
the acoustic communication of anurans.
Federico Bolaiios is a professor of Herpetology at the School of Biology of the University of Costa
Rica, curator of the Herpetology collection at Museo de Zoologia, and a member of the International
Union for Conservation and Nature (Amphibian, Conservation Breeding, and Viper Specialist
Groups). Federico’s M.Sc. dissertation focused on the natural history and population ecology of
Oophaga granulifera. His primary interest involves the behavioral ecology of amphibians, but he
has also participated in taxonomic studies, including the description of nine species of amphibians.
Federico became a professor when amphibian declines were first being detected and has since
dedicated most of his research efforts to this topic. He has mentored more than 35 graduate students
in Biology at UCR. He has authored more than 70 publications, including book chapters and peer
reviewed papers in scientific journals, and has served as a book editor.
322 December 2019 | Volume 13 | Number 2 | e215
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
13(2) [General Section]: 323-354 (e216).
urn:lsid:zoobank.org:pub:E0578CD4-6843-42A9-9E23-25B8C23FC1DA
Three new species of day geckos (Reptilia: Gekkonidae:
Cnemaspis Strauch, 1887) from isolated granite cave
habitats in Sri Lanka
1*Suranjan Karunarathna, 7Anslem de Silva, **Madhava Botejue, *Dinesh Gabadage, ®Lankani
Somaratna, ‘*Angelo Hettige, ‘Nimantha Aberathna, °®Majintha Madawala, **Gayan Edirisinghe,
‘Nirmala Perera, ‘*Sulakshana Wickramaarachchi, °Thilina Surasinghe, '*Niranjan Karunarathna,
‘°Mlendis Wickramasinghe, ‘Kanishka D.B. Ukuwela, and ‘*Aaron M. Bauer
'Nature Explorations and Education Team (NEET), No: B-1 / G-6, De Soysapura Flats, Moratuwa 10400, SRI LANKA Amphibia and Reptile
Research Organization of Sri Lanka (ARROS), 15/1, Dolosbage Road, Gampola 20500, SRI LANKA °Biodiversity Conservation Society (BCS),
150/6, Stanly Thilakaratne Mawatha, Nugegoda 10250, SRI LANKA *Central Environmental Authority (CEA), 104, Denzil Kobbekaduwa Mawatha,
Battaramulla 10120, SRI LANKA °Zoology Division, Department of National Museums, Colombo 07, SRI LANKA °Young Zoologist Association of
Sri Lanka (YZA), Department of National Zological Gardens, Dehiwala 10350, SRI LANKA ‘Youth Exploration Society of Sri Lanka (YES), Royal
Botanical Garden, Peradeniya 20400, SRI LANKA 8Victorian Herpetological Society (VHS), P.O. box 4208, Ringwood, VIC 3134, AUSTRALIA
°Department of Biological Sciences, Bridgewater State University, Bridgewater, MA 02325, USA '°Herpetological Foundation of Sri Lanka (HFS),
31/5, Alwis Town, Hendala, Wattala 11300, SRI LANKA ''Department of Biological Sciences, Faculty of Applied Sciences, Rajarata University of
Sri Lanka, Mihintale 50300, SRI LANKA '*Department of Biology, Center for Biodiversity and Ecosystem Stewardship, Villanova University, 800
Lancaster Avenue, Villanova, Pennsylvania 19085, USA
Abstract.—Three new day gecko species of the genus Cnemaspis Strauch, 1887 are described from three
isolated granite cave habitats with rock walls in Bambaragala (Ratnapura District), Dimbulagala (Polonnaruwa
District), and Mandaramnuwara (Nuwara-Eliya District) in Sri Lanka based on morphometric and meristic
characters. All of these new species are assigned to the kandiana clade based on morphology. These species
are small (28-35 mm SVL) in size and may be differentiated from all other Sri Lankan congeners by a suite
of distinct morphometric and meristic characters. Each of these species described herein are categorized
as Critically Endangered (CR) under IUCN Red List criteria. At the microhabitat scale, they are restricted to
wet, cool, and shady granite caves and rock outcrops in isolated forested areas with limited anthropogenic
disturbance. Further, these habitats are located in all three main bioclimatic zones (wet, intermediate, dry)
and all three geographic peneplains (first, second, third) of Sri Lanka. Due to their restricted distributions
(as point endemics), the habitats of these specialist species are vulnerable to fragmentation, edge effects,
and anthropogenic activities. Therefore, these isolated forest patches in Sri Lanka are in need of special
conservation attention and management.
Keywords. Climate condition, endangered species, habitat specialist, isolated forest, point endemic, range restriction,
systematics, taxonomy
Citation: Karunarathna S, de Silva A, Botejue M, Gabadage D, Somaratna L, Hettige A, Aberathna N, Madawala M, Edirisinghe G, Perera N,
Wickramaarachchi S, Surasinghe T, Karunarathna N, Wickramasinghe M, Ukuwela KDB, Bauer AM. 2019. Three new species of day geckos (Reptilia:
Gekkonidae: Cnemaspis Strauch, 1887) from isolated granite cave habitats in Sri Lanka. Amphibian & Reptile Conservation 13(2) [General Section]:
323-354 (e216).
Copyright: © 2019 Karunarathna et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [At-
tribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in
any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 28 May 2019; Accepted: 4 December 2019; Published: 31 December 2019
Introduction sequently, Cnemaspis ranks as the second most diverse
gecko genus in the world, next to Cyrtodactylus (Gris-
Taxonomic descriptions and phylogenetic revisions in
the past decade have rapidly increased the number of
day gecko species recognized in the genus Cnemaspis,
bringing the global species richness to more than 155
(Karunarathna et al. 2019a,b; Uetz et al. 2019a). Con-
Correspondence. *suranjan.karu@gmail.com
Amphib. Reptile Conserv.
mer et al. 2014; Uetz et al. 2019a). However, extensive
molecular phylogenetic analyses have questioned the
monophyly of Cnemaspis which is represented by three
geographically disjunct groups from South Asia, Tropi-
cal Africa, and Southeast Asia (Gamble et al. 2012; Py-
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
ron et al. 2013a; Zheng and Wiens 2016). Cnemaspis
geckos are diminutive, slender-bodied geckos that pos-
sess prominent forward and upwardly-directed eyes with
round pupils, broad flattened heads, and elongate slender
digits that are bent at an angle with entire subdigital la-
mellae (Vidanapathirana et al. 2014; Wood et al. 2017;
Karunarathna et al. 2019a). These geckos are adapted for
a scansorial mode of life, with most being rupicolous,
while a few are arboreal or ground-dwelling with crepus-
cular behavior (Das 2005). They appear to be microhabi-
tat specialists with occupancy limited to shaded surfaces
of rocks, caves, trees, abandoned buildings, buildings as-
sociated with caves, wattle and daub houses, and rock
walls within suitable habitats where the cryptic morphol-
ogy and body coloration help them camouflage with their
surroundings (Smith 1935; Karunarathna et al. 2019b).
Much like continental south Asia, as well as the Indo-
Malayan realm, the species richness of Cnemaspis in Sri
Lanka has grown rapidly by at least eight-fold, from four
to 33 species (Deraniyagala 1953; Manamendra-Arach-
chi et al. 2007; Wicramasinghe and Munindradasa 2007;
Karunaratha and Ukuwela 2019). As such, Cnemaspis
has become the most diverse gecko genus on the island,
with 100% endemism. Through molecular phylogenetic
analyses of mitochondrial and nuclear DNA, Agarwal et
al. (2017) demonstrated the presence of two distinct Cne-
maspis Clades in Sri Lanka (kandiana and podihuna), and
indicated the presence of cryptic diversity within four
species (C. alwisi Wickramasinghe and Munidradasa
2007; C. kumarasinghei Wickramasinghe and Munidra-
dasa 2007; C. latha Manamendra-Arachchi, Batuwita,
and Pethiyagoda 2007, and C. podihuna Deraniyagala
1944). The aforementioned studies emphasized the need
for detailed studies on Cnemaspis taxonomy using a
combination of both morphological characteristics and
molecular phylogenetics. As indicated by recent stud-
ies in Sri Lanka, the faunistic surveys of under-explored
habitats followed by rigorous phylogenetic analyses will
further augment the species richness of Cnemaspis (Bau-
er et al. 2007; Agarwal et al. 2017; Karunarathna et al.
2019b). In light of this, we conducted field excursions in
various isolated localities in Sri Lanka. Here, we describe
three new Cnemaspis species (based on morphometric
and meristic characters) discovered from three such sites
which span all three bioclimatic zones and geological pe-
neplains of Sri Lanka.
Materials and Methods
Field sampling and specimens. Field surveys across 122
different locations in Sri Lanka covered several geograph-
ic areas (e.g., dry zone, intermediate zone, and wet zone).
At each location, gecko species found were surveyed and
documented with special attention on the focal genus. On
average, 12 surveyor-hours per location were devoted to
the survey. Museum acronyms follow Sabaj (2016) and
Uetz et al. (2019b). The type materials discussed in this
Amphib. Reptile Conserv.
paper are deposited in the National Museum of Sri Lanka
(NMSL), Colombo, Sri Lanka. Specimens were caught
by hand and were photographed in life. They were eutha-
nized using halothane and fixed in 10% formaldehyde for
two days, washed in water, and then transferred to 70%
ethanol for long-term storage. Tail tips were collected as
tissue samples before fixation and were stored in 95%
ethanol under relatively cool conditions (20—25 °C). For
comparison, 424 Cnemaspis specimens (catalogued and
uncatalogued) representing all recognized Sri Lankan
species were examined, including all type specimens
housed at the National Museum, Sri Lanka (NMSL), The
Natural History Museum, London (BMNH), and in the
private collections of Anslem de Silva (ADS) and Aaron
Bauer (AMB), which had been deposited in the NMSL.
Specimens that formerly belonged to the Wildlife Heri-
tage Trust (WHT) collection and bear WHT numbers are
currently deposited in the NMSL, catalogued under their
original numbers. Specimens in this study were collected
during a survey of lizards in Sri Lanka under permit num-
bers WL/3/2/1/14/12 and WL/3/2/42/18 (a and b), issued
by the Department of Wildlife Conservation, and under
permit numbers FRC/5 and FRC/6, issued by the Forest
Department of Sri Lanka. Additional information on the
morphology and natural history of Sri Lankan Cnemaspis
species was extracted from the relevant literature (Bauer
et al. 2007; Manamendra-Arachchi et al. 2007; Wick-
ramasinghe and Munindradasa 2007; Vidanapathirana
et al. 2014; Wickramasinghe et al. 2016; Batuwita and
Udugampala 2017; Agarwal et al. 2017; Batuwita et al.
2019; Karunarathna et al. 2019a,b; de Silva et al. 2019).
Assignment of unidentified specimens to the three new
Species was based on their morphometric and meristic
characters (Tables 1-9), color patterns, and geographic
isolation (Fig. 1; Table 10). The new species described in
the present paper are completely new and have not been
included in previous phylogenies of the genus (see A gar-
wal et al. 2017; Karunarathna et al. 2019b).
Morphometric characters. Forty morphometric mea-
surements were taken using a Mitutoyo digital Vernier
calliper (to the nearest 0.1 mm), and detailed observa-
tions of scales and other structures were made through
Leica Wild M3Z and Leica EZ4 dissecting microscopes.
The following symmetrical morphometric characters
were taken on the left side of the body: eye diameter
(ED), horizontal diameter of eye ball; orbital diameter
(OD), greatest diameter of orbit; eye to nostril length
(EN), distance between anteriormost point of orbit and
posterior border of nostril; snout length (ES), distance
between anteriormost point of orbit and tip of snout;
snout to nostril length (SN), distance between tip of
snout and anteriormost point of nostril; nostril width
(NW), maximum horizontal width of nostrils; eye to ear
distance (EE), distance between posterior border of eye
and anteriormost point of ear opening; snout to axilla
distance (SA), distance between axilla and tip of snout;
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Contour 600 m
Climate zone boundary
Dry zone
_ Intermediate zone
, Wet zone
;
L " Kilometers
WeGe 1984 UTM Zone 44h
Fig. 1. Currently known distribution of Cnemaspis dissanay-
akai sp. nov. (square) from Dimbulagala; Cnemaspis kawmin-
iae sp. nov. (circle) from Mandaramnuwara; and Cnemaspis
kotagamai sp. nov. (triangle) from Bambaragala, Sri Lanka.
ear length (EL), maximum length of ear opening; interor-
bital width (IO), shortest distance between left and right
supraciliary scale rows; inter-ear distance (IE), distance
across head between the two ear openings; head length
(HL), distance between posterior edge of mandible and
tip of snout; head width (HW), maximum width of head
between the ears and the orbits; head depth (HD), maxi-
mum height of head at the level of the eye; jaw length
(JL), distance between tip of snout and corner of mouth;
internarial distance (IN), smallest distance between in-
ner margins of nostrils; snout to ear distance (SED), dis-
tance between tip of snout and anteriormost point of ear;
upper-arm length (UAL), distance between axilla and
the angle of the elbow; lower-arm length (LAL), dis-
tance from elbow to wrist with palm flexed; palm length
(PAL), distance between wrist (carpus) and tip of longest
finger excluding the claw; length of digits I-V of manus
(DLM), distance between juncture of the basal phalanx
with the adjacent digit and the tip of the digit, excluding
the claw; snout-vent length (SVL) distance between tip
of snout and anterior margin of vent; trunk length (TRL),
distance between axilla and groin; trunk width (TW),
Amphib. Reptile Conserv.
maximum width of body; trunk depth (TD), maximum
depth of body; femur length (FEL), distance between
groin and knee; tibia length (TBL), distance from knee to
heel with ankle dorsiflexed; heel length (HEL), distance
between ankle (tarsus) and tip of longest toe (excluding
the claw) with both foot and tibia flexed; length of pedal
digits I-V (DLP), distance between juncture of the basal
phalanx with the adjacent digit and the digit tip, exclud-
ing the claw; tail length (TAL), distance between anterior
margin of the vent and tail tip; tail base depth (TBD),
maximum height of tail base; tail base width (TBW),
widest point of tail base.
Meristic characters. Thirty discrete characters were ob-
served and recorded using Leica Wild M3Z and Leica
EZ4 dissecting microscopes on both the left (L) and the
right (R) sides of the body (reported in the form L/R):
number of supralabials (SUP) and infralabials (INF) be-
tween the first labial scale and corner of mouth; number of
interorbital scales (INOS), between left and right supra-
ciliary scale rows; number of postmentals (PM) bounded
by chin scales, 1“ infralabial on the left and right and
the mental; number of chin scales (CHS), scales touching
medial edge of infralabials and mental between juncture
of 1‘ and 2" infralabials on the left and right; number of
supranasal (SUN) scales between nares; presence of the
postnasal (PON) scales posterior to naris; presence of the
internasal (INT) scale between supranasals; number of
supraciliary scales (SUS) above eye; number of scales
between eye and tympanum (BET) from posteriormost
point of orbit to anteriormost point of tympanum; num-
ber of canthal scales (CAS), number of scales from pos-
teriormost point of naris to anteriormost point of orbit;
total lamellae on manus I-V (SLM) counted from first
proximal enlarged scansor greater than twice width of the
largest palm scale, to distalmost lamella at tip of digits;
number of dorsal paravertebral granules (PG) between
pelvic and pectoral limb insertion points along a straight
line immediately left of vertebral column; number of
midbody scales (MBS) from the center of mid-dorsal
row diagonally towards the ventral scales; number of
midventral scales (MVS) from the first scale posterior to
the mental to last scale anterior to vent; number of belly
scales (BLS) across venter between the lowest rows of
granular dorsal scales; total lamellae on pes I-V (SLP),
counted from first proximal enlarged scansor greater than
twice the width of the largest heel scale, to distalmost
lamella at tip of digits; number of precloacal pores (PCP)
anterior to the cloaca; number of femoral pores (FP)
present on femur; numbers of non-pored proximal femo-
ral scales (PFS) counted from proximal ends of femo-
ral pore rows to precloacal pores; numbers of non-pored
distal femoral scales (DFS) counted from distal ends of
femoral pore rows to knee; interfemoral scales (IFS)
number of non-pored scales between femoral pores on
both femurs. Additional evaluations included the texture
[keeled (KD) or smooth (SM)] of the ventral scales, the
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
texture [heterogeneous (HET) or homogeneous (HOM)|
of the dorsal scales, the number of spinous scales on the
flanks (FLSP), and characteristics such as appearance of
the caudal scales (except in specimens with regenerated
tails). Coloration was determined from digital images of
living specimens and also from direct observations in the
field.
Distribution and natural history. The new species de-
scribed herein were collected during field surveys con-
ducted in various habitats (e.g., dry mixed semi-evergreen
forest and tropical wet-evergreen) of Sri Lanka (Fig. 1;
Table 10). During these surveys, behavioral and other
aspects of natural history of the focal species were ob-
served through opportunistic and non-systematic means.
The ambient and substrate temperatures were measured
using a standard thermometer and an N19 Q1370 infrared
thermometer (Dick Smith Electronics, Shanghai, China),
respectively. The relative humidity and light intensity
were measured with a QM 1594 multifunction environ-
ment meter (Digitek Instruments Co., Ltd., Hong Kong,
China). To record elevation and georeference species lo-
cations, an eTrex® 10 GPS (Garmin) was used. Sex was
determined by the presence in males (M) or absence in
female (F) of hemipenal bulges, and precloacal and fem-
oral pores. The conservation status of each new species
was evaluated using the 2001 IUCN Red List Categories
and Criteria version 3.1 (IUCN 2012).
Statistical analyses of morphometric characteristics.
Principal Component Analyses (PCA) were performed
with the conventional singular value decomposition
method using variance-covariance stricture as the cross-
products matrix to extract 10 principal components
(package: PCAMethods, function:pca; Stacklies et al.
2007). The species used for these analyses are: Cnemas-
pis dissanayakai sp. nov., Cnemaspis ingerorum, Cne-
maspis kallima, Cnemaspis kawminiae sp. nov., Cne-
maspis kotagamai sp. nov., Cnemaspis kumarasinghei,
Cnemaspis latha, and Cnemaspis gotaimbarai groups
due to their close resemblances. All morphometric mea-
surements of the three new species were normalized
to the snout-vent length (SVL). The matrix containing
Table 1. Principal component scores and corresponding species.
original morphometric variables were Pareto scaled
(square-root unit variance) and centered. Subsequently,
pairwise ordination plots were generated for the first
four principal components (PC), which explained nearly
80% of the cumulative variance, where each individual
PC accounted for at least 8% of the overall variance. To
visualize species separation in the ordination space, con-
vex hulls were placed around PC scores corresponding to
each species (Wickham 2016). In addition, PC loadings
were examined against each of the selected PC axes to
understand the relationships between the original mor-
phometric variables and the PC axes. This examination
also revealed which morphometric variables were most
distinct among the different species. In addition to the
collective analyses of the eight aforementioned conge-
nerics, three separate PCAs were run which focused on
three species groups based on their close morphological
resemblances: (1) Cnemaspis kotagamai sp. nov., Cne-
maspis ingerorum, and Cnemaspis kallima; (2) Cnemas-
pis dissanayakai sp. nov., Cnemaspis latha, and Cne-
maspis kumarasinghei;, and (3) Cnemaspis kawminiae
sp. nov., Cnemaspis gotaimbarai, and Cnemaspis kuma-
rasinghei. The aforementioned analyses used statistical
program R (R Core Team 2019) and RStudio integrated
development environment (R Studio Team 2018). Ordi-
nation plots were produced using the following statisti-
cal applications and R packages: PAST version 3.14 and
geplot2 (Hammer et al. 2001).
Results
Analyses of morphometric data for all eight species.
The PCA resulted in 10 PCs that accounted for 98% of
the variability of the original morphometric variables;
among these, PC 1-4 (35.64%, 19.48%, 14.35%, and
8.70%, respectively) cumulatively explained 78% of the
overall variability (Fig. 2). Trunk and upper-arm lengths
had greater loadings on PC1 while tail length, orbital di-
ameter, snout-to-nostril length, and the lengths of the 4"
and 5" pestal digits had greater loadings on PC2. Heel
length, snout-to-axilla length, eye diameter, inner-ear dis-
tance, eye-to-nostril distance, trunk width, and length of
the 4" finger had higher loadings on PC3; whereas trunk
Average scores for principal components
Species
PCl1 PC2
C. kotagamai 0.31 0.52
C. dissanayakai -0.50 0.20
C. kawminiae 0.40 -0.05
C. kumarasinghei 0.12 -0.28
C. gotaimbarai 0.44 -0.47
C. ingerorum 0.15 0.24
C. latha -0.60 -0.03
C. kallima -0.33 -0.13
Amphib. Reptile Conserv.
326
PC3 PC4 PCS PC6
0.31 0.12 0.16 0.00
0.17 -0.22 0.01 -0.10
-0.23 -0.27 0.13 0.34
0.09 -0.02 0.25 -0.21
0.20 0.06 -0.20 -0.06
-0.63 0.10 -0.09 -0.19
0.025 0.37 -0.03 0.17
0.07 -0.14 -0.23 0.03
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
A C B oO
3 & 0.25-
& 05 7
5 a : is
> = 0.00-
c) ok, 6 f
= a =
4 O.0- t RE 4 mal a 0.25"
a oO Zz
ow on “0.50
oO oO
a -05 a
“0 5 4 i ‘ ‘
“1.0 “0.5 0.0 05 1.0 “0.5 0.0 os
PC1 35.64 % of vanance PC1 35.64 % of vanance
x rr)
i AS D 7
oily o = ‘ =
a 35 - =
Ee WP _ — 5 al 3 oF es)
oS ; oO C oa CS
a sa en a ee se
oo -D.2 =
s f = A
3 “0.25 on 050°
a : a
-0.50- : he ; ; “0.75: ; : Mv
1.0 “0.5 00 0.5 0.5 0.0 05
PC1 35.64 % of variance PG2 19.48% of vanance
E ona F He
om ow
e 0.25 i & 0.25- 4
5 . xi Gl oO Fa - Wy r 4 a)
peal ST = 7 a, = —4">
2 0.00- ‘ * -L + : 2 0.00- + <i
[ri] Lea] a a
Lia] Lewy
oo o
“0.25 - “0.25 -
tT TT
O Oo
a a
0.50" — 0.50 , ; _ & :
“0.5 0.0 05 0.75 0.50 0.25 0.00 0.25
PC2 19.48 % of variance PC3 14.35 % of variance
species |) kotagamai |) dissanayakai a kawminiae “BS kumarasinghei ) gotaimbarai GF ingerorum | latha ) kallima
. H 084 or |
sie 0.08-+ soa | o
! [ *, | 9.0504
- ~ Oe ce ee ee se i = ee | = L e !
S naal! © 0.044 _ t Bn bocce ets ;
3” ; z |. =. =2 = -_| 20,0254 * |
= = Li eS na Sie | 2 ' i
‘i = a | @ ee ee 2 ew as eae |
cL ‘a | | [as 1 !
= 0.00 & 0.00- r-- | # 0.000-+ |
m9 Ho bees £2 cee Eee mcpuae sea
line! te] Go } H " aa! Se }
~ 0.04 Romatick ec cada oe Sec ees es | =0.0255 |
2 dae Ribs na ade Sack 12 | es |
| |
b- ----- rh ----- <b ------r------ bh.
0.08 Pen sukioe ela oe Sepia Ee] |
D084 --- ---p 2-2-2 52-22 ep a-a- ee | i }
; [Pe ntl A ee Sewn Oe Ne ered ee oat a | | ry |
“0.16 “0.08 0.00 0.08 O16 0.16 -0.08 0.00 0.08 0.16 “0.16 -0.08 0.00 0.08 0.16
PC1 (49.3% explained var.) PC1 (42.5% explained var.) PC1 (64.5% explained var.)
species @ kotagamal © dissanayakai (] kawminiae % kumarasinghei gotaimbarai <A, ingerorum = {§j latha © kallima
Fig. 2. (A-F) PCA Ordination plots for multivariate morphometric analyses (all pairwise ordination plots for PC1 through PC4
are shown), (G) Scatter plot of PCA between Cnemaspis kotagamai sp. nov. (filled circles), Cnemaspis ingerorum (triangles),
and Cnemaspis kallima (filled diamonds), (H) Scatter plot of PCA between Cnemaspis dissanayakai sp. nov. (circles), Cnemas-
pis latha (filled squares), and Cnemaspis kumarasinghei (stars), (I) Scatter plot of PCA between Cnemaspis kawminiae sp. nov.
(squares), Cnemaspis gotaimbarai (filled triangles), and Cnemaspis kumarasinghei (stars).
and tail lengths had higher loadings on PC4 (Tables 1—2).
The ordination for PC1 and PC2 provided the strongest
evidence for morphometric-based species separation—
expect for Cnemaspis kawminiae, C. kumarasinghei, C.
kallima, and C. latha, whose separation was most evident
in ordination between PC1 and PC4 (Fig. 2). In addition,
PC1 and PC3 supported separation of species based on
morphometrics relatively well.
Amphib. Reptile Conserv.
327
Analyses of morphometric data for separate species
groups. PCA of morphometric measurements of Cne-
maspis kotagamai sp. nov., Cnemaspis ingerorum, and
Cnemaspis kallima indicated the presence of three well
separated species (Fig. 2). Cnemaspis kotagamai sp. nov.
and Cnemaspis kallima were clearly separated from the
PC2 axis, while Cnemaspis ingerorum and Cnemaspis
kallima were seprated along PC1. The PC1 and PC2 axes
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
Table 2. Morphometric variables and corresponding PC load- Table 3. Morphometric data of holotype and two paratypes of
ings. Cnemaspis kotagamai sp. nov. from Bambaragala, Ratnapura
Measurements PCL PC2 PC3 PCA District, Sri Lanka.
ED -0.14 0.02 0.15 0.00 NMSL NMSL NMSL
2019.15.01 2019.15.02 2019.15.03
OD -0.22 0.21 0.06 -0.03 Measurenents —_—_—_———————————————————
Holotype Paratype Paratype
EN 0.01 -0.14 0.16 -0.04 (Male) (Male) (Female)
ES -0.08 -0.05 -0.12 -0.19 SVL 29 8 31.1 39-6
SN -0.13 0.18 0.03 0.06 TRL 12.6 123 12.5
NW 0.02 0.04 -0.07 — -0.04 TW 5.4 53 54
EE 0.10 -0.05 0.03 -0.10 TD 3.4 3.4 3.4
SA 0.15 -0.40 0.18 -0.15 TAL 33.5 33.8 31.1
EL -0.08 0.14 G20 SEIS TBW 3.3 31 2.9
IO -0.22 0.05 0.07 0.06 TBD 2.9 2.9 2.7
IE 0.20 0.02 0.15 -0.03 ED 1.9 1.9 1.8
HL 0.18 -018 0.05 -0.27 OD 3.2 3.3 3.1
HW 016 “011 <013» 0.04 EN 2.8 2.8 27
HD 0.08 -014 -0.24 -0.07 ES 3.6 3.5 ay
JL 0.00, SO.108 <0:17 0.06 on me a LS
NW 0.2 03 0.2
IN -0.16 0.11 0.05 0.03
EE 2.5 2.5 23
SED -0.23 0.08 -0.01 0.12
SA 12.9 12.7 11.8
UAL O29 -=6:07 0.03 0.15 me es a ws
LAL O15 -0.26 -0.03 0.18 in se Ae ae
PAL -0.04 0.07 -0.28 -0.13 - 38 69 38
DLM -1 -0.06 -0.02 -0.03 -0,27 HL 83 83 82
DLM-2 -0.01 — -0.06 0.00 -0.22 Hw 45 Aa 45
DLM-3 -0.10 -0.03 0.08 -0.17 HD 28 26 OF
DLM-4 -0.15 -0.06 0.14 -0.18 JIL 49 48 49
DLM-5 -0.17 0.02 0.12 -0.06 IN 1.6 1.6 1.4
TRL 0.22 -0O.13 -0.25 -0.48 SED 8.7 8.6 8.7
TW -0.22 0.11 0.14 -0.15 UAL 3.8 34) 39
TD -0.16 0.11 0.10 -0.09 LAL 3.4 3:3 Ee
FEL -0.16 -0.07 0.05 -0.13 PAL 3.2 3.2 3.2
TBL 1020 «003 ST DLM (i) 1.4 1.4 1.3
HEL 0.01 0.06 -048 0.22 DLM (it) 1.9 18 18
DLP-1 0.04 007 -031 -0.14 oe 2.5 25 2.6
DLP-2 0.24 013 -020 -0.10 DEM) ay uh
DLM (vy) phe 23 23
DLP-3 O19 -0.03 -0.15 -0O11
FEL 5.8 5.8 5.7
DLP-4 -0.19 0.16 -0.24 0.04
TBL 52 5.1 49
DLP-5 4) 3 0.21 -0.20 -0.02
HEL 48 45 47
TAL O15 -0.62 -0.20 0.24 DLP (i) a i Vs
TBW -0.14 -0.03 -0.01 0.22 DLP (ii) ae ro a4
TBD -O.11 0.05 0.01 0.21 DLP (iii) 9 28 07
DLP (iv) 3.8 3.9 3.7
DLP (v) 3.5 33 3.5
Amphib. Reptile Conserv. 328 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
mn
= i
a:
: ;
*
a
i
Be
fi
ae
fh te
j-
Ri saaras r >
ee ee es eg
ae Seah: a
i, eel
oa
Fig. 3. Holotype male of Cnemaspis kotagamai sp. nov. (NMSL 2018.15.01). (A) Dorsal head, (B) lateral head, (C) ventral head,
(D) heterogeneous dorsal scales, (E) scales on lateral surface of trunk, (F) smooth ventral scales, (G) cloacal characters with pre-
cloacal pores and femoral pores, (H) lamellae on manus, (I) lamellae on pes, (J) keeled dorsal scalation of tail, (IX) lateral side of
tail, and (L) very small smooth subcaudals. Photos: Suranjan Karunarathna.
explained 49.5% and 27.3% of the observed variation,
respectively. Analysis of morphometric measurements of
Cnemaspis dissanayakai sp. nov., Chemaspis latha, and
Cnemaspis kumarasinghei similarly indicated the pres-
ence of three well separated species (Fig. 2). Cnemas-
pis dissanayakai sp. nov. and Cnemaspis kumarasinghei
Amphib. Reptile Conserv.
were well separated in the PC1 axis while the former was
clearly separated from Cnemaspis latha in the PC2 axis.
The PC1 and PC2 axes explained 42.5% and 32.5% of
the observed variation, respectively. PCA analysis of the
morphometric measurements of Cnemaspis kawminiae
sp. nov., Cnemaspis gotaimbarai, and Cnemaspis kuma-
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
— ee *.
® a.
Se.
uw oo [Pa
Fig. 4. Holotype male of Cnemaspis kotagamai sp. nov. (NMSL 2018.07.01) in life in-situ in Bambaragala. (A) Dorsal view of the
full body, and (B) ventral view with scattered yellow coloration. Photos: Suranjan Karunarathna.
rasinghei indicated the presence of three well separated
species (Fig. 2). Cnemaspis kawminiae sp. nov. was
clearly separated from Cnemaspis gotaimbarai along
the PC2 axis, while it was distinguished from C. kuma-
rasinghei also in the PC2 axis. The PCI and PC2 axes
explained 64.5% and 17.1% of the observed variation,
respectively.
Systematics
Cnemaspis kotagamai sp. nov. Karunarathna, de Sil-
va, Boteyue, Surasinghe, Wickramasinghe, Ukuwela &
Bauer
Kotagama’s Day Gecko (English)
Kotagamage Diva-seri Hoona (Sinhala)
Kotagamavin Pahalpalli (Tamil)
Figs. 3-5; Tables 3-4
urn:lsid:zoobank.org:act:35801F43-7148-4590-BE38-4214C8905646
Holotype. NMSL 2019.15.01, adult male, 29.8 mm SVL
(Fig. 3), collected from a granite cave Bambaragala, Pal-
Amphib. Reptile Conserv.
lebedda, Ratnapura District, Sabaragamu Province, Sri
Lanka (6.512978°N, 80.750306°E, WGS1984; elevation
127 m; around 1100 hrs) on 18 January 2019 by Suranjan
Karunarathna and Anslem de Silva.
Paratypes. NMSL 2019.15.02, adult male, 31.1 mm
SVL, and NMSL 2019.15.03, adult female, 32.6 mm
SVL, collected from a granite cave in Bambaragala,
Pallebedda, Ratnapura District, Sabaragamuwa Prov-
ince, Sri Lanka (6.517261°N, 80.752692°E, WGS1984;
elevation 132 m; around 1200 hrs) on 18 January 2019
by Suranjan Karunarathna and Anslem de Silva.
Diagnosis. Cnemaspis kotagamai sp. nov. may be read-
ily distinguished from its Sri Lankan congeners by a
combination of the following morphological and mer-
istic characteristics as well as color patterns: maximum
SVL 32.6 mm; dorsum with heterogeneous, smooth in-
termixed with weakly keeled granular scales; 2/2 supra-
nasals, one internasal, 2/2 postnasals; 3—4 enlarged post-
mentals; postmentals bounded by 5-6 chin scales; chin,
gular, pectoral, and abdominal scales smooth, subimbri-
cate; 21—22 belly scales across midbody; 6—7 well-devel-
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Table 4. Meristic data of holotype and two paratypes of Cne-
maspis kotagamai sp. nov. from Bambaragala, Ratnapura Dis-
trict, Sri Lanka.
NMSL NMSL NMSL
2019.15.01 2019.15.02 2019.15.03
Counts Se a ee ee
Holotype Paratype Paratype
(Male) (Male) (Female)
FLSP (L/R) 6/7 6/6 7/7
SUP (L/R) 8/8 8/8 7/8
INF (L/R) FEL 8/7 7/7
INOS 31 29 31
PM 4 4 3
CHS 6 5 6
SUN (L/R) 2/2 2/2 2/2
PON (L/R) 2/2 2/2 2/2
INT l 1 l
SUS (L/R) 12/12 14/13 12/12
BET (L/R) 22122 21/19 21/22
CAS (L/R) 11/10 11/10 10/10
TLM (i) (L/R) 9/9 10/9 10/10
TLM (ii) (L/R) 12/12 12/11 12/12
TLM (iii) (L/R) 14/14 14/13 13/13
TLM (iv) (L/R) 15/15 14/14 14/13
TLM (v) (L/R) 12/12 11/12 12/12
PG 114 119 116
MBS 84 79 81
MVS 134 137 131
BLS 21 21 22
TLP (1) (L/R) 9/9 8/9 8/8
TLP (ii) (L/R) 14/14 13/14 14/14
TLP (iii) (L/R) 16/16 16/16 15/16
TLP (iv) (L/R) 17/17 17/18 18/17
TLP (v) (L/R) 16/16 15/15 16/15
PCP. 1 1 -
FP (L/R) 5/5 4/4 -
PFS (L/R) 12/13 11/12 -
DFS (L/R) 2/2 4/6 -
oped tubercles on posterior flank; 114—119 paravertebral
granules linearly arranged; one precloacal pore, 4-5 fem-
oral pores in males, separated by 11-13 unpored proxi-
mal femoral scales, 2—6 unpored distal femoral scales;
131-137 ventral scales; 79-84 midbody scales; subcau-
dals smooth, median row comprising an irregular series
of diamond-shaped, small scales; 7-8 supralabials; 7—8
infralabials; 13-15 total lamellae on 4" digit of manus,
and 17-18 total lamellae on 4" digit of pes.
Comparisons with other Sri Lankan species. Among
species of the C. kandiana clade sensu Agarwal et al.
(2017), Cnemaspis kotagamai sp. nov. differs by hav-
ing heterogeneous (versus homogeneous) dorsal scales
Amphib. Reptile Conserv.
from C. amith Manamendra-Arachchi et al. 2007, C.
gotaimbarai Karunarathna et al. 2019b, C. kumarasing-
hei Wickramasinghe and Munindradasa 2007, C. latha
Manamendra-Arachchi et al. 2007, and C. nandimithrai
Karunarathna et al. 2019b; it can also be diagnosed from
C. butewai Karunarathna et al. 2019b, C. kandiana (Ke-
laart, 1852), C. kivulegedarai Karunarathna et al. 201 9b,
C. menikay Manamendra-Arachchi et al. 2007, C. pava
Manamendra-Arachchi et al. 2007, C. pulchra Manamen-
dra-Arachchi et al. 2007, C. retigalensis Wickramasing-
he and Munindradasa 2007, C. samanalensis Wickrama-
singhe and Munindradasa 2007, C. si/vula Manamendra-
Arachchi et al. 2007, C. tropidogaster (Boulenger, 1885),
and C. upendrai Manamendra-Arachchi et al. 2007 by
having smooth (versus keeled) pectoral scales. The new
species differs from C. kallima Manamendra-Arachchi et
al. 2007 by having more midbody scales (79-84 versus
67-74), presence of more paravertebral granules (114—
119 versus 99-107), by having fewer precloacal pores
(1 versus 3-4), and having fewer tubercles on the poste-
rior flank (6—7 versus 12-15). It differs from C. ingero-
rum Batuwita et al. 2019 by having more ventral scales
(131-137 versus 88—95) and more paravertebral granules
(114-119 versus 93-101).
Among species of the C. podihuna clade sensu Agar-
wal et al. (2017), Cnemaspis kotagamai sp. nov. differs
by the absence of clearly enlarged, hexagonal or subhex-
agonal subcaudal scales from the following species: C.
alwisi Wickramasinghe and Munindradasa 2007, C. ans-
/emi Karunarathna and Ukuwela 2019, C. gemunu Bauer
et al. 2007, C. godagedarai de Silva et al. 2019, C. hiti-
hami Karunarathna et al. 2019b, C. kandambyi Batuwita
and Udugampala 2017, C. kohukumburai Karunarathna
et al. 2019b, C. molligodai Wickramasinghe and Munin-
dradasa 2007, C. nilgala Karunarathna et al. 2019, C.
phillipsi Manamendra-Arachchi et al. 2007, C. podihuna
Deraniyagala, 1944, C. punctata Manamendra-Arachchi
et al. 2007, C. rajakarunai Wickramasinghe et al. 2016,
C. rammalensis Vidanapathirana et al. 2014, and C. scal-
pensis (Ferguson 1877).
Description of Holotype (NMSL 2019.15.01). An adult
male, 29.8 mm SVL and 33.5 mm TAL. Body slender,
relatively long (TRL/SVL ratio 42.2%). Head relatively
small (HL/SVL ratio 28.0% and HL/TRL ratio 66.2%),
narrow (HW/SVL ratio 15.3% and HW/HL ratio 54.6%),
depressed (HD/SVL ratio 9.5% and HD/HL ratio 33.9%),
and distinct from neck. Snout relatively long (ES/HW ra-
tio 78.4% and ES/HL ratio 42.8%), less than twice eye
diameter (ED/ES ratio 52.5%), more than half length of
jaw (ES/JL ratio 72.1%), snout slightly concave in lateral
view; eye relatively small (ED/HL ratio 22.5%), larger
than the ear (EL/ED ratio 44.4%), pupil rounded; orbit
length greater than eye to ear distance (OD/EE ratio
127.8%) and length of IV digit of manus (OD/DLM IV
ratio 111.8%); supraocular ridges moderately developed;
ear opening small (EL/HL ratio 10.0%), deep, taller than
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
wide, larger than nostrils; two rows of scales separate or-
bit from supralabials; interorbital distance is greater than
snout length (IO/ES ratio 101.7%), shorter than head
length (IO/HL ratio 43.5%); eye to nostril distance great-
er than the eye to ear distance (EN/EE ratio 109.5%).
Dorsal surface of the trunk with smooth scales inter-
mixed with weakly keeled heterogeneous granules, 114
paravertebral granules; 134 midventral scales, smooth; 84
midbody scales; 6/7 weakly developed tubercles on the
flanks; ventrolateral scales irregular, enlarged; granules
on snout smooth and raised, larger than those on interor-
bital and occipital regions; canthus rostralis nearly absent,
11/10 smooth oval scales from eye to nostril; scales of the
interorbital region circular and smooth; tubercles present
both on the sides of the neck and around the ear; ear open-
ing vertically oval, slanting from anterodorsal to postero-
ventral, 22/22 scales between anterior margin of the ear
opening and the posterior margin of the eye. Supralabials
8/8, infralabials 7/7, becoming smaller towards the gape.
Rostral scale wider than long, partially divided (80%) by
a median groove, contact with first supralabial. Nostrils
separated by 2/2 enlarged supranasals with one internasal;
no enlarged scales behind the supranasals. Nostrils oval,
dorsolaterally orientated, not in contact with first supra-
labials; 2/2 postnasals, smooth, larger than nostrils, par-
tially in contact with first supralabial.
Amphib. Reptile Conserv.
Wark
Fig. 5. General habitat of Cnemaspis kotagamai sp. nov. at Bambaragala isolated forest hill, Ratnapura District, Sri Lanka. (A) Rock
outcrop habitat, (B) abandoned cave building, and (C) deep and tall granite tunnel. Photos: Madhava Botejue.
Mental sub-rhomboid in shape, as wide as long, poste-
riorly in contact with four enlarged postmentals (smaller
than mental, and larger than chin scales); postmentals in
contact and bordered posteriorly by six unkeeled chin
scales (smaller than nostrils), in contact with the 1* in-
fralabial; ventral scales smaller than chin scales. Smooth,
rounded, juxtaposed scales on the chin and the gular re-
gion; pectoral and abdominal scales smooth, subimbri-
cate to imbricate towards precloacal region, abdominal
scales slightly larger than dorsals; 21 belly scales across
venter; smooth scales around vent and base of tail,
subimbricate; one precloacal pore; 5/5 femoral pores;
12/13 unpored proximal femoral scales on each side; 2/2
enlarged distal femoral scales. Regenerated tail of holo-
type a little longer than the snout-vent length (TAL/SVL
ratio 112.7%); hemipenal bulge greatly swollen (TBW
3.3 mm), heterogeneous scales on the dorsal aspect of
the tail directed backwards, spine-like tubercles present
at the base of tail; tail with 4—5 enlarged flattened obtuse
scales forming whorls; a large, blunt post-cloacal spur
on each side, dorsoventrally flattened and narrow; sub-
caudals smooth and small, subrhomboidal, arranged in a
single median series.
Forelimbs very short, slender (LAL/SVL ratio 11.4%
and UAL/SVL ratio 12.7%); hind limbs long, tibia shorter
than femur (TBL/SVL ratio 17.3% and FEL/SVL ratio
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
19.4%). Anterior surface of upper arm with keeled and
less imbricate scales; dorsal, posterior, and ventral sur-
face smooth, scales of the anterior surface twice as large
as those of the other surfaces; anterior and dorsal surfaces
of lower arm with keeled and less imbricate scales, ven-
tral and posterior surfaces with unkeeled imbricate scales,
scales on the anterior surface of upper arm and lower arm
twice the size of those of other aspects. Scales on dorsal
and ventral surfaces of femur smooth, those on anterior
and posterior surfaces keeled, scales on the ventral surface
twice the size of those of other aspects. Dorsal, anterior,
and posterior surfaces of tibia with keeled and weakly im-
bricate scales, ventral surface with smooth, subimbricate
scales, scales of the ventral surface twice as large as those
on other aspects. Dorsal and ventral surfaces of manus and
pes with keeled granules; dorsal surfaces of digits with
granular scales. Digits elongate and slender with inflected
distal phalanges, all bearing slightly recurved claws. Sub-
digital lamellae entire (except divided at first interphalan-
gial joint), unnotched; total lamellae on manus (left/right):
digit I (9/9), digit II (12/12), digit IM (14/14), digit IV
(15/15), digit V (12/12); total lamellae on pes (left/right):
digit I (9/9), digit II (14/14), digit II (16/16), digit IV
(17/17), digit V (16/16); interdigital webbing absent; rela-
tive length of left manual digits: I (1.4 mm), II (1.9 mm),
V (2.3 mm), II (2.5 mm), IV (2.9 mm); relative length of
left pedal digits: I (1.2 mm), I (2.1 mm), HI (2.9 mm), V
(3.5 mm), IV (3.8 mm).
Variation of the type series. The SVL of adult speci-
mens in the type series of Cnemaspis kotagamai sp. nov.
(n = 3) ranges from 29.8 to 32.6 mm; interorbital scales
29-31; supraciliaries above the eye 12—14; scales from
eye to tympanum 19-22; canthal scales 10—11; tubercles
on posterior flank 6—7; chin scales 5—6; ventral scales
131-137 (Tables 3-4); midbody scales 79-84; paraverte-
bral granules 114—119; belly scales across venter 21—22:
femoral pores in males 4—5:; unpored proximal femoral
scales in males 11-13; unpored distal femoral scales in
males 2—6; total lamellae on digit of the manus: digit I
(9-10), digit IT (11-12), digit HI (13-14), digit IV (13-
15), digit V (11-12); total lamellae on digit of the pes:
digit I (8-9), digit IT (13-14), digit HI (15-16), digit IV
(17-18), digit V (15-16).
Color of living specimens. Dorsum of head, body, and
limbs generally brown; one broad, yellow vertebral
stripe running form occiput to tail (Fig. 4); five irregular
blackish-brown paravertebral blotches present; occipital
area with a ‘W’-shaped dark marking. Tail dark brown
dorsally, with 11 faded black cross-bands; pupil circu-
lar and black with the surrounding margins yellow and
orange, supraciliaries yellowish; two black postorbital
stripes on each side; an oblique black line between the
eye and nostril on either side; supralabials and infralabi-
als yellowish with tiny black spots; chin and gular scales
dirty white, without dark spots; pectoral, abdominal, clo-
acal, and subcaudal scales immaculate cream; dorsum of
Amphib. Reptile Conserv.
limbs with faded black patches; manus and pes alternat-
ing black and cream-white crossbands.
Color of preserved specimens. Dorsally blackish-brown
with five distinct dark, irregular brown blotches (Fig. 3);
supralabials and infralabials dirty white; chin and gular
scales grey; ventral surface uniformly dirty white in col-
or, with some scales on thigh, tail base, and arms with
dark brown margins.
Etymology. The specific epithet is an eponym Latinized
(kotagamai) in the masculine genitive singular, honoring
prominent Sri Lankan scientist (ornithologist), Sarath Wi-
malabandara Kotagama (Emeritus Professor of the Uni-
versity of Colombo) for his valuable contributions towards
biodiversity conservation and management in Sri Lanka.
Distribution and naturalhistory. The type locality, Bam-
baragala forest (6.509086—6.522369°N and 80.742731—
80.759386°E; Ratnapura District, Sabaragamuwa Prov-
ince), is located in the lowland (southern intermediate
bioclimatic zone) where tropical moist semi-evergreen
forests comprise the dominant vegetation type (Guna-
tileke and Gunatileke 1990). The forest acreage is ~50 ha
and relatively isolated by anthropogenically-altered flat
lands. Bambaragala lies at an elevation of 110—178 m asl.
The mean annual rainfall of 1,500—2,000 mm Is received
mainly during the southwest monsoon (May—Septem-
ber), while the mean annual temperature 1s 27.8—29.6 °C.
Bambaragala is rich in granite rock caves with over 30
identified caves. Cnemaspis kotagamai sp. nov. appeared
to be a very rare species in Bambaragala, as only five
individuals were recorded during the survey. This species
was located in a granite cave on vertical surfaces, 4 m in
height, within the forested area (Fig. 5). The microhabitat
of C. kotagamai sp. nov. was poorly illuminated (light in-
tensity: 385-469 Lux), relatively moist (relative humid-
ity: 71-88%), canopy-shaded (canopy cover: 65—80%),
and relatively cool (ambient temperature: 29.8—31.3 °C
and substrate temperature: 27.8—28.6 °C). The new spe-
cles was sympatric with several other gecko species: Ge-
hyra mutilata, Hemidactylus depressus, H. frenatus, and
H. parvimaculatus. No eggs were observed.
Conservation status. Application of the IUCN Red List
criteria indicates that C. kotagamai sp. nov. is Critically
Endangered (CR), due to having an area of occupancy
(AOO) <10 km? (four locations, 0.13 km? in total assum-
ing a 100 m radius around the georeferenced location) and
an extent of occurrence (EOO) <100 km? (0.37 km/’) in
Sabaragamuwa Province [Applicable criteria B2-b (111)].
Remarks. Cnemaspis kotagamai sp. nov. most closely
resembles C. ingerorum (southern dry zone, ~85 m asl)
and C. kallima (northern wet zone, ~600 m asl) morpho-
logically, the type localities of these species are separated
by ~63 km (Sandagala in Tissamaharamaya) and ~115
km (Gammaduwa in Matale) straight line distances from
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
Fig. 6. Holotype male of Cnemaspis dissanayakai sp. nov. (NMSL 2018.20.01). (A) Dorsal head, (B) lateral head, (C) ventral
head, (D) homogeneous dorsal scales, (E) scales on lateral surface of trunk, (F) smooth ventral scales, (G) cloacal characters with
precloacal pores and femoral pores, (H) lamellae on manus, (I) lamellae on pes, (J) smooth dorsal scalation of tail, (IX) lateral side
of tail, and (L) very small smooth subcaudals. Photos: Suranjan Karunarathna.
Bambaragala in Pallebedda (Fig. 1). Also see the com- —- Dissanayakage Diva-seri Hoona (Sinhala)
parison with other species for more details. Dissanayakavin Pahalpalli (Tamil)
Figs. 6-8; Tables 5—6
Cnemaspis dissanayakai sp. nov. Karunarathna, de
Silva, Madawala, Karunarathna, Wickramasinghe, urn:|sid:zoobank.org:act:7A BF9B28-7D04-4296-BDB5-ECEA07B1 F965
Ukuwela & Bauer
Dissanayaka’s Day Gecko (English) Holotype. NMSL 2019.20.01, adult male, 28.6 mm SVL
Amphib. Reptile Conserv. 334 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Table 5. Morphometric data of holotype and two paratypes of
Cnemaspis dissanayakai sp. nov. from Dimbulagala, Polonna-
ruwa District, Sri Lanka.
NMSL NMSL NMSL
2019.20.01 2019.20.02 2019.20.03
Measurements Se ee
Holotype Paratype Paratype
(Male) (Male) (Female)
SVL 28.6 28.2 29.4
TRL 11.1 11.2 11.0
TW 55 5.4 oer
TD 3.6 3.4 33
TAL 31.1 31.2 34.4
TBW 25 2.7 2.8
TBD Di 23 Die
ED 1.9 19 1.9
OD 3.3 3.1 3.1
EN 2.4 2.4 2:3
ES 3.6 a7 3.6
SN 1.3 1.4 1.4
NW 0.2 O72 0.2
EE 2.5 oa 2,5
SA esa 12.9 12.8
EL 0.8 0.8 0.9
IO 3.6 3.6 mie
IE 3.8 3:7 se,
HL 9.0 8.9 8.9
HW 43 45 4.4
HD 2.4 25 2
JL 5D 5.6 5.6
IN 1.6 1.6 1.6
SED 8.1 8.2 8.2
UAL 4.6 4.6 4.6
LAL 4.2 4.2 4.2
PAL 3.2, Bee 33
DLM (1) 1.6 1.6 ies
DLM (ii) 1.8 1.8 1.9
DLM (iit) 2.8 2 Dal
DLM (iv) 33 Se 3.4
DLM (v) 25 2.4 2.6
FEL 5.6 5.6 36
TBL Saf Sl 5.5
HEL 3.9 3.8 3.8
DLP (1) 1.3 15 Ls
DLP (11) a2 3.2 343
DLP (iii) 3.6 3.6 SF
DLP (iv) 4 4l 4.2
DLP (v) are 3.8 3,7
Amphib. Reptile Conserv.
Table 6. Meristic data of holotype and two paratypes of Cne-
maspis dissanayakai sp. nov. from Dimbulagala, Polonnaruwa
District, Sri Lanka.
NMSL NMSL NMSL
2019.20.01 2019.20.02 2019.20.03
Counts
Holotype Paratype Paratype
(Male) (Male) (Female)
FLSP (L/R) 7/6 7/7 6/6
SUP (L/R) 7/7 7/7 7/7
INF (L/R) 7/7 7/7 7/7
INOS 31 29 29
PM 3 3 3
CHS ) 6 6
SUN (L/R) 212 2/2 2/2
PON (L/R) 1/1 1/1 1/1
INT 1 1 l
SUS (L/R) 16/16 16/17 16/15
BET (L/R) 22/23 21/21 21/22
CAS (L/R) 11/12 11/11 11/11
TLM (i) (L/R) 10/10 10/10 10/10
TLM (ii) (L/R) 13/12 1272 12/12
TLM (iit) (L/R) 13/13 12/13 12/12
TLM (iv) (L/R) a2i24 21/21 21/21
TLM (v) (L/R) 14/14 13/14 14/13
PG 105 107 105
MBS 98 94 95
MVS 118 120 119
BLS 17 LF 19
TLP (i) (L/R) 8/8 8/9 8/8
TLP (it) (L/R) 13/14 13/13 13/13
TLP (ii) (L/R) 16/16 16/15 16/16
TLP (iv) (L/R) 22/21 21-21 21/21
TLP (v) (L/R) 17/16 17/17 17/17
PCP 2 2 -
FP (L/R) 5/4 4/4 -
PFS (L/R) 10/10 11/10 -
DFS (L/R) 7/5 FT -
(Fig. 6), collected from a large granite cave in the shaded
forest of Dimbulagala, Polonnaruwa District, North-
Central Province, Sri Lanka (7.872931°N, 81.135569°E,
WGS1984; elevation 129 m; around 1600 hrs) on 12 July
2018 by Suranjan Karunarathna and Anslem de Silva.
Paratypes. NMSL 2019.20.02, adult female, 29.4 mm
SVL, and NMSL 2019.20.03, adult male, 28.2 mm SVL,
collected from moss covered granite cave in Dimbula-
gala, Polonnaruwa District, North-Central Province, Sri
Lanka (7.851358°N, 81.141675°E, WGS1984; elevation
135 m; around 1200 hrs) on 12 July 2018 by Suranjan
Karunarathna and Anslem de Silva.
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
Diagnosis. Cnemaspis dissanayakai sp. nov., may be
readily distinguished from its Sri Lankan congeners by
a combination of the following morphological and mer-
istic characteristics: maximum SVL 29.4 mm; dorsum
with homogeneous, subconical granular scales; one in-
ternasal, 2/2 supranasals, 1/1 postnasals; 29-31 interor-
bital scales; 15—17 supraciliaries, 11-12 canthal scales,
21-23 eye to tympanum scales; three enlarged postmen-
tals; postmentals bounded by 6—7 chin scales; chin with
smooth granules, gular, pectoral, and abdominal scales
smooth, subimbricate; 17 belly scales across the venter;
6—7 well developed tubercles on posterior flank; 105—107
linearly arranged paravertebral granules; two precloacal
pores, 4—5 femoral pores on each side in males separated
by 10-11 unpored proximal femoral scales, 5-7 unpored
distal femoral scales; 118—120 ventral scales; 94—98 mid-
body scales; subcaudals smooth, median row small, in an
irregular series of diamond-shaped scales; 7/7 supralabi-
als; 7/7 infralabials; 21-22 total lamellae on 4" digit of
manus, and 21—22 total lamellae on 4" digit of pes.
Comparisons with other Sri Lankan species. Among
species of the C. kandiana clade sensu Agarwal et al.
(2017), Cnemaspis dissanayakai sp. nov. differs from C.
butewai, C. ingerorum, C. kallima, C. kandiana, C. ki-
vulegedarai, C. kotagamai sp. nov., C. menikay, C. pava,
C. pulchra, C. retigalensis, C. samanalensis, C. silvula,
C. tropidogaster, and C. upendrai by having homoge-
neous (versus heterogeneous) dorsal scales; from C.
amith by having smooth (versus keeled) pectoral scales;
from C. kumarasinghei, C. latha, and C. nandimithrai
by having more paravertebral granules (105-107 ver-
sus 61-68, 72-79, and 95-99, respectively), and from
by having more total lamellae on digit [V of manus and
digit IV of pes (21-22 versus 16-18, 17-18, and 19-20,
respectively); from C. gotaimbarai by having fewer
paravertebral granules (86-92 versus 117-121), fewer
ventral scales (107—114 versus 129-138), and fewer total
lamellae on digit IV of manus and digit IV of pes (15-16
versus 19-20).
Among species of the C. podihuna clade sensu Agar-
wal et al. (2017), Cnemaspis dissanayakai sp. nov. dif-
fers by the absence of clearly enlarged, hexagonal or
subhexagonal subcaudal scales from the following spe-
cies: C. alwisi, C. anslemi, C. gemunu, C. hitihami, C.
kandambyi, C. kohukumburai, C. molligodai, C. nilgala,
C. phillipsi, C. podihuna, C. punctata, C. rajakarunai, C.
rammalensis, and C. scalpensis.
Description of Holotype (NMSL 2019.20.01). An adult
male, 28.6 mm SVL, and 31.1 mm TAL. Body slender,
relatively short (TRL/SVL ratio 38.8%). Head relatively
long (HL/SVL ratio 31.5% and HL/TRL ratio 81.1%),
very narrow (HW/SVL ratio 15.1% and HW/HL ratio
48.0%), depressed (HD/SVL ratio 8.2% and HD/HL ra-
tio 26.2%), and distinct from neck. Snout relatively long
(ES/HW ratio 82.2% and ES/HL ratio 39.5%), less than
Amphib. Reptile Conserv.
twice eye diameter (ED/ES ratio 52.8%), more than half
length of jaw (ES/JL ratio 65.2%), snout slightly con-
cave in lateral view; eye relatively small (ED/HL ratio
20.8%), twice as large as the ear (EL/ED ratio 43.6%),
pupil rounded; orbit length greater than eye to ear dis-
tance (OD/EE ratio 131.0%) and also shorter than length
of IV digit of manus (OD/DLM IV ratio 99.7%); supra-
ocular ridges not prominent; ear opening very small (EL/
HL ratio 9.1%), deep, taller than wide, larger than nos-
trils; two rows of scales separate orbit from supralabials:
interorbital distance slightly shorter than snout length
(IO/ES ratio 99.7%), less than half of head length (1O/
HL ratio 39.4%); eye to nostril distance slightly shorter
than the eye to ear distance (EN/EE ratio 95.2%).
Dorsal surface of trunk with homogeneous, subconi-
cal granules; 105 paravertebral granules; 118 mid-ventral
scales, smooth; 98 midbody scales; 7/6 well developed
tubercles on flanks; ventrolateral scales not enlarged:
granules on snout strongly keeled, larger than those on
interorbital and occipital regions; canthus rostralis nearly
absent, 11/12 smooth round scales from eye to nostril;
scales of the interorbital region oval and smooth; 2/2
small and blunt tubercles present on sides of neck, and
around ear; ear opening vertically oval, backward slant-
ed, 22/23 scales between anterior margin of ear opening
and posterior margin of eye. Supralabials 7/7, infralabi-
als 7/7, becoming smaller towards the gape. Rostral scale
wider than long, partially divided (70%) by a median
groove, in contact with first supralabial. Nostrils sepa-
rated by 2/2 enlarged supranasals with one internasal; no
enlarged scales behind supranasals. Nostrils oval, dorso-
laterally orientated, not in contact with first supralabials;
1/1 postnasals, smooth, larger than nostrils, partially in
contact with first supralabial.
Mental subtriangular, as wide as long, posteriorly in
contact with three enlarged postmentals (smaller than
mental, and larger than chin scales); postmentals in con-
tact and bordered posteriorly by seven smooth chin scales
(smaller than nostrils), in contact only with 1* infralabials;
ventral scales smaller than chin scales; smooth, rounded,
juxtaposed scales on the chin and gular region; pectoral
and abdominal scales smooth, subimbricate to imbricate
towards precloacal region, abdominal scales slightly larger
than dorsals; 17 belly scales across venter; scales around
vent and base of tail smooth, subimbricate; two precloacal
pores; 5/4 femoral pores; 10/10 unpored proximal femo-
ral scales on each side; 7/5 enlarged distal femoral scales.
Original tail of holotype longer than snout-vent length
(TAL/SVL ratio 108.7%); tail base greatly swollen (TBW
2.5 mm), heterogeneous scales on dorsum of the tail di-
rected backwards, spine-like tubercles along tail; tail with
4-6 enlarged flattened obtuse scales forming whorls; a
small, blunt post-cloacal spur on each side, dorsoventrally
flattened and narrow; median series of smooth, irregular,
oval to rhomboid subcaudals.
Forelimbs moderately short, slender (LAL/SVL ra-
tio 14.7% and UAL/SVL ratio 15.9%); hind limbs long,
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
tibia barely longer than the femur (TBL/SVL ratio 19.7%
and FEL/SVL ratio 19.6%). Dorsal, anterior, and pos-
terior surfaces of upper arm and lower arm with keeled
and less imbricate scales than ventrals, ventral surfaces
smooth, less imbricate scales than ventrals, scales of the
anterior surface twice as large as those of the other sur-
faces. Scales on dorsal, posterior, and ventral surfaces of
femur smooth and granular, anterior surface with keeled
subimbricate scales, anterior surface twice as large as
those of the other aspects; dorsal, anterior and posterior
surfaces of tibia with keeled and subimbricate scales,
ventral scales smooth, subimbricate, twice as large as
those of the other limb surfaces. Manus and the pes with
keeled granules dorsally and ventrally; dorsum of dig-
its with granular scales; digits elongate and slender with
inflected distal phalanges, all bearing slightly recurved
claws. Subdigital lamellae entire (except divided at first
interphalangial joint), unnotched; total lamellae on ma-
nus (left/right): digit I (10/10), digit IT (13/12), digit I
(13/13), digit IV (22/21), digit V (14/14); total lamellae
on pes (left/right): digit I (8/8), digit II (13/14), digit II
(16/16), digit IV (22/21), digit V (17/16); interdigital
webbing absent; relative length of digits of left manus: I
(1.6 mm), II (1.8 mm), V (2.5 mm), III (2.8 mm), IV (3.3
‘ai &
mm); relative length of digits of left pes: I (1.5 mm), II
(3.2 mm), III (3.6 mm), V (3.9 mm), IV (4.1 mm).
Variation of the type series. The SVL of adult speci-
mens in the type series of Cnemaspis dissanayakai sp.
nov. (n = 3) ranges from 28.2 to 29.4 mm; interorbital
scales 29-31; supraciliaries above the eye 15—17; scales
from eye to tympanum 21—23; canthal scales 11-12; tu-
bercles on posterior flank 6—7; chin scales 6—7; ventral
scales 118-120; midbody scales 94-98; paravertebral
granules 105-107 (Tables 5-6); belly scales across ven-
ter 17-19; femoral pores 4-5; unpored proximal femor-
als 10-11; unpored distal femoral scales 5—7; total lamel-
lae on digit of the manus: digit I (8-9), digit II (13-14),
digit III (15-16), digit IV (21-22); total lamellae on digit
of the pes: digit I (8-9), digit IT (13-14), digit II (15-16),
digit IV (21-22), digit V (16-17).
Color of living specimens. Dorsum of the head, body,
and limbs generally dull brown, varying from light ma-
roon to light brown, five faded and irregular ‘W’-shaped
brown markings on the trunk; 4—5 cream vertebral blotch-
es (Fig. 7); an oblique black line between eye and nostrils
on either side, two straight, dark brown postorbital stripes
et |
© a
Fig. 7. Holotype male of Cnemaspis dissanayakai sp. nov. (NMSL 2018.20.01) in life in-situ in Dimbulagala. (A) Dorsal view of
the full body, and (B) ventral view with dirty white coloration. Photos: Suranjan Karunarathna.
Amphib. Reptile Conserv.
337
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
aes "i a E Pi. f
Fig. 8. General habitat of Cnemaspis dissan
ayakai sp. nov. at Dimbulagala isolated hill forest, Polonnaruwa District, Sri La
, . ai ae
nka.
(A) Complete view of the mountain, (B) abandoned ancient cave building in Kosgahaulpatha, and (C) deep and tall granite tunnel.
Photos: Madhava Botejue and Ashan Geeganage.
extend from eyes posteroventrally, and a faded spot pres-
ent in the occipital area. Tail grey-pink dorsally, with S—7
irregular faded brown cross-bands; pupil is circular and
black with the surrounding orange, with supraciliaries
being light brownish; supralabials dirty whitish dusted
with black; infralabials greyish dusted with black; mid-
gular scales are yellowish; pectoral, abdominal, cloacal,
and subcaudal scales white without markings; dorsum of
limbs with irregular brown patches and lines; manus and
pes with black and cream cross white stripes on dorsum.
Color of preserved specimens. Dorsum dark brown
with grey, faded indistinct irregular brown markings;
vertebral blotches cream. Venter dirty white with some
scales on throat, abdomen, thigh, tail base, and arms with
dark brown margins (Fig. 6).
Etymology. The specific epithet is an eponym Latinized
(dissanayakai) in the masculine genitive singular, honoring
Dissanayaka Mudiyanselage Karunarathna (born in Nilga-
la, Bibila) — father of the first author (Suranjan Karunara-
thna) for his encouragement, financial support for research,
and for allowing SK to pursue his interest in wildlife.
Distribution and natural history. The type local-
ity, Dimbulagala (7.843919-7.876344°N, 81.105603-—
Amphib. Reptile Conserv.
81.156442°E), situated in the Polonnaruwa District, North
Central Province (northeast dry bioclimatic zone) of Sri
Lanka, supports tropical dry-mixed evergreen forests (Gu-
natileke and Gunatileke 1990), and is ~1,000 ha in size.
The mean annual rainfall of 1,500—2,000 mm is received
mainly during the northeast monsoon (November—Febru-
ary). The mean annual temperature of the area is 28.9—30.2
°C, and its elevation range is 120-250 m asl. According
to preliminary investigations, Cnemaspis dissanayakai sp.
nov. appeared to be very rare in Dimbulagala. The survey
of 35 ha recorded two (+ 0.1) geckos per surveyor-hour of
effort. This species was restricted to rocky surfaces and
granite caves in shaded forested areas, and old abandoned
buildings inside the forest (Fig. 8). These microhabitats
were well-shaded (light intensity: 594-648 Lux), rela-
tively humid (relative humidity: 65-90%), and moderately
warm (ambient temperature: 30.2—31.9 °C and substrate
temperature 27.5—28.6 °C). The new species was observed
to occur in sympatry with the following gecko species:
Calodactylodes illingworthorum, Gehyra mutilata, Hemi-
dactylus depressus, H. frenatus, H. hunae, H. parvimac-
ulatus, and H. triedrus. Older and newly laid eggs were
observed in granite rock crevices, usually laid in clusters
of three. The eggs were pure white in color and almost
spherical in shape (mean diameter 4.9 + 0.02 mm), with a
slightly flattened side attached to the rocky substrate.
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
_ - ‘3 A
re r
Fig. 9. Holotype male of Cnem
aspis kawminiae sp. nov. (NMSL 2018.18.01). (A) Dorsal head, (B) lateral head, (C) ventral head,
\
Haat
=|
(D) homogeneous dorsal scales, (E) scales on lateral surface of trunk, (F) smooth ventral scales, (G) cloacal characters with precloa-
cal pores and femoral pores, (H) lamellae on manus, (I) lamellae on pes, (J) smooth dorsal scalation of tail, (IX) lateral side of tail,
and (L) very small subcaudals. Photos: Suranjan Karunarathna.
Conservation status. Application of the IUCN Red
List criteria indicates that C. dissanayakai sp. nov. is
Critically Endangered (CR) due to having an area of
occupancy (AOO) <10 km? (four locations, 0.13 km? in
total assuming a 100 m radius around the georeferenced
location) and an extent of occurrence (EOO) <100 km?
(4.08 km?) in North Central Province [Applicable crite-
ria B2-b (ii1)].
Amphib. Reptile Conserv.
Remarks. Cnemaspis dissanayakai sp. nov. most closely
resembles C. kumarasinghei (east intermediate zone) and
C. latha (southern intermediate zone) morphologically.
The type localities of these species are separated by ~105
km (Maragala in Monaragala, ~500 m asl) and ~90 km
(Bandarawela in Badulla, ~700 m asl) straight line dis-
tances from Dimbulagala in Polonnaruwa (Fig. 1). Also
see the comparison with other species for more details.
December 2019 | Volume 13 | Number 2 | e216
Table 7. Morphometric data of holotype and two paratypes of
Cnemaspis kawminiae sp. nov. from Mandaramnuwara, Nu-
wara-Eliya District, Sri Lanka.
Measurements
SVL
TRL
TW
TD
TAL
TBW
TBD
IN
SED
UAL
LAL
PAL
DLM (i)
DLM (ii)
DLM (iii)
DLM (iv)
DLM (v)
FEL
TBL
HEL
DLP (i)
DLP (ii)
DLP (iii)
DLP (iv)
DLP (v)
Amphib. Reptile Conserv.
Three new species of Cnemaspis from Sri Lanka
NMSL NMSL NMSL
2019.18.01 2019.18.02 2019.18.03
Holotype Paratype Paratype
(Male) (Male) (Female)
33.7 33.2 5556,
16.4 14.9 16.2
RO) 5.4 5.4
3.4 3.2 3:3
36.1 42.7 38.0
3.4 3.4 3:2
2:9 2.8 2.7
1.5 1.5 1.4
3.1 29 Dd
3.1 SZ. Sl
4.3 45 4.8
2 1.3 1s
0.3 0.3 0.3
2 Sie 3,2
14.9 14.8 14.9
0.9 0.9 0.9
2.9 29) 2)
37 af 3:3
9.9 9.4 10.4
3:5 5.3 a2
3.8 3.6 3.6
5.9 5.8 5.8
1.3 1.3 1.3
8.3 8.2 8.0
45 43 43
45 4.5 4.5
4.6 4.2 4.2
2.1 2.2 2.2
235 2S, 2.6
2.6 27 2.6
3.0 29) 3.0
Ze zie 2.2
6.5 6.3 6.5
6.1 6.1 6.1
5:3 5.8 6.1
2.1 221 2.1
3.0 2 3.0
3.5 3.5 3.5
3.8 3.8 3.8
3.6 3.8 3.6
Table 8. Meristic data of holotype and two paratypes of Cne-
maspis kawminiae sp. nov. from Mandaramnuwara, Nuwara-
Eliya District, Sri Lanka.
NMSL NMSL NMSL
2019.18.01 2019.18.02 2019.18.03
Counts
Holotype Paratype Paratype
(Male) (Male) (Female)
FLSP (L/R) 8/7 77 8/7
SUP (L/R) 8/8 8/8 8/7
INF (L/R) 7/7 8/7 77
INOS eA | 20 22
PM 3 3 3
CHS 5 a 5
SUN (L/R) 2/2 2/2 2/2
PON (L/R) 2/2 2/2 2/2
INT 1 1 |
SUS (L/R) 10/10 10/10 10/9
BET (L/R) 22/20 21/21 22/20
CAS (L/R) 10/11 10/10 10/10
TLM (i) (L/R) 10/9 10/9 10/10
TLM (ii) (L/R) 13/13 12/12 13/12
TLM (iii) (L/R) 14/13 14/14 14/14
TLM (iv) (L/R) 15/14 15/15 14/14
TLM (v) (L/R) 13/14 14/14 14/13
PG 89 92 86
MBS 78 76 76
MVS 107 108 114
BLS 21 17 19
TLP (i) (L/R) 9/9 10/9 10/10
TLP (ii) (L/R) 12/13 12/12 12/12
TLP (iii) (L/R) 16/15 16/16 15/15
TLP (iv) (L/R) 16/16 15/16 15/16
TLP (v) (L/R) 14/14 14/15 15/15
PCP 2 2 -
FP (L/R) 4/4 4/4 2
PFS (L/R) 12/11 12/13 2
ROME __ Gis _ Ee A _t
Cnemaspis kawminiae sp. nov. Karunarathna, de Silva,
Gabadage, Karunarathna, Wickramasinghe, Ukuwela &
Bauer
Kawmini’s Day Gecko (English)
Kawminige Divaseri Hoona (Sinhala)
Kawminivin Pahalpalli (Tamil)
Figs. 9-11; Tables 7-8
urn:lsid:zoobank.org:act: 12E14150-D66F-471C-98B1-E805C5A 9244F
Holotype. NMSL 2019.18.01, adult male, 33.7 mm SVL
(Fig. 9), collected from a moss-covered granite wall in
Mandaramnuwara, bordering Pidurutalagala Mountain
range, Nuwara-Elitya District, Central Province, Sri
340 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Lanka (7.033558°N, 80.798794°E, WGS1984; elevation
1,600 m asl, around 1100 hrs) on 14 December 2018 by
Suranjan Karunarathna and Anslem de Silva.
Paratypes. NMSL 2019.18.02, adult male, 33.2 mm SVL
and NMSL 2019.18.03, adult female, 35.2 mm SVL, col-
lected from a small granite cave Mandaramnuwara, bor-
dering Pidurutalagala Mountain, Nuwara-Eliya District,
Central Province, Sri Lanka (7.020600°N, 80.788639°E,
WGS1984; elevation 1,658 m asl, around 1400 hrs) col-
lected on 14 December 2018 by Suranjan Karunarathna
and Anslem de Silva.
Diagnosis. Cnemaspis kawminiae sp. nov., may be read-
ily distinguished from its Sri Lankan congeners by a
combination of the following morphological and meristic
characteristics: maximum SVL 35.2 mm; dorsum with
homogeneous flat granular scales; one internasal, 2/2 su-
pranasals and 2/2 postnasals; 20—22 interorbital scales;
9-10 supraciliaries, 10—11 canthal scales, 20-22 eye to
tympanum scales; three enlarged postmentals; postmen-
tals bounded by five chin scales; chin with smooth and
round granules, gular, pectoral, and abdominal scales
smooth, subimbricate; 17—21 belly scales across the ven-
ter; 7-8 weakly developed tubercles on posterior flank:
86-92 linearly arranged paravertebral granules; two pre-
cloacal pores in males, 4/4 femoral pores on each side
in males separated by 11—13 unpored proximal femoral
scales, 6-7 unpored distal femoral scales; 107-114 ven-
tral scales; 76-78 midbody scales; subcaudals smooth,
median row small, in an irregular series of sub-rhomboid
shaped scales; 7-8 supralabials; 7-8 infralabials; 14—15
total lamellae on 4" digit of manus, and 15-16 total la-
mellae on 4" digit of pes.
Comparisons with other Sri Lankan species. Among
species of the C. kandiana clade sensu Agarwal et al.
(2017), Cnemaspis kawminiae sp. nov. differs from C.
butewai, C. ingerorum, C. kallima, C. kandiana, C. ki-
vulegedarai, C. kotagamai sp. nov., C. menikay, C. pava,
C. pulchra, C. retigalensis, C. samanalensis, C. silvula, C.
tropidogaster, and C. upendrai by having homogeneous
(versus heterogeneous) dorsal scales; from C. amith by
having smooth (versus keeled) pectoral scales; from C.
gotaimbarai, C. kumarasinghei, and C. dissanayakai
sp. nov. by having fewer ventral scales (107-114 versus
129-138, 120-134 and 118-120, respectively), and also
from C. kumarasinghei and C. dissanayakai sp. nov. by
having fewer midbody scales (76—78 versus 87-94 and
94-98, respectively), from C. gotaimbarai by having
fewer paravertebral granules (86—92 versus 117-121),
from C. latha by having more paravertebral granules
(86—92 versus 72—79), and more belly scales (17-21 ver-
sus 13-15); from C. nandimithrai by having fewer belly
scales (17-21 versus 25-27) and by having fewer total
lamellae on digit IV of pes (15—16 versus 19-20).
Amphib. Reptile Conserv.
The new species, Cnemaspis kawminiae sp. nov., also
clearly differs from the following species of the C. po-
dihuna clade sensu Agarwal et al. (2017): C. alwisi, C.
anslemi, C. gemunu, C. godagedarai, C. hitihami, C.
kandambyi, C. kohukumburai, C. molligodai, C. nilgala,
C. phillipsi, C. podihuna, C. punctata, C. rajakarunai, C.
rammalensis, and C. scalpensis by the absence (versus
presence) of clearly enlarged, hexagonal or subhexago-
nal subcaudal scales.
Description of Holotype (NMSL 2019.18.01). An adult
male, 33.7 mm SVL, and 36.1 mm TAL. Body slender,
relatively long (TRL/SVL ratio 48.7%). Head relatively
small (HL/SVL ratio 29.4% and HL/TRL ratio 60.4%),
relatively broad (HW/SVL ratio 16.4% and HW/HL
ratio 55.6%), weakly depressed (HD/SVL ratio 11.2%
and HD/HL ratio 38.1%), and distinct from neck. Snout
relatively short (ES/HW ratio 78.4% and ES/HL ratio
43.6%), slightly less than three times eye diameter (ED/
ES ratio 34.4%), more than half length of jaw (ES/JL ra-
tio 73.3%), snout slightly concave in lateral view; eye
very small (ED/HL ratio 15.0%), larger than ear (EL/ED
ratio 59.7%), pupil rounded; orbit length slightly smaller
than eye to ear distance (OD/EE ratio 97.2%) and lon-
ger than length of IV digit of manus (OD/DLM IV ra-
tio 105.4%); supraocular ridges weakly prominent; ear
opening very small (EL/HL ratio 9.0%), deep, taller than
wide, larger than nostrils; two rows of scales separate or-
bit from supralabials; interorbital distance less than snout
length (IO/ES ratio 67.7%), head length three times lon-
ger than interorbital distance ([O/HL ratio 29.5%); eye to
nostril distance subequal to eye to ear distance (EN/EE
ratio 98.1%).
Dorsal surface of trunk with homogeneous, flat granu-
lar and smooth scales; 112 paravertebral granules; 149
midventral scales, keeled; 69 midbody scales; 6/6 well
developed tubercles on flanks; ventrolateral scales ir-
regularly enlarged; granules on snout strongly keeled,
larger than those on interorbital and occipital regions;
canthus rostralis nearly absent, 9/10 smooth round scales
from eye to nostril; scales of the interorbital region oval
and smooth; small and blunt tubercles present on sides of
neck, and around ear; ear opening vertically oval, slant-
ing from anterodorsal to posteroventral, 20/19 scales be-
tween anterior margin of ear opening and the posterior
margin of eye. Supralabials 8/7, infralabials 7/7, becom-
ing smaller towards the gape. Rostral scale wider than
long, partially divided (90%) by a median groove, in con-
tact with first supralabial. Nostrils separated by 2/2 en-
larged supranasals with one internasal, 2/2 postnasals; no
enlarged scales behind supranasals. Nostrils oval, dorso-
laterally orientated, not in contact with first supralabials.
Mental subtriangular, as wide as long, posteriorly in
contact with three enlarged postmentals (smaller than
mental, and lager than chin scales); postmentals in con-
tact and bordered posteriorly by five smooth chin scales
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
(smaller than nostrils), in contact only with 1 and 2"4
infralabials; ventral scales smaller than chin scales.
Smooth, oval, juxtaposed scales on the chin and gular
region; pectoral and abdominal scales smooth, subim-
bricate to imbricate towards precloacal region, abdomi-
nal scales slightly larger than dorsals; 21 belly scales
across venter; scales around vent and base of tail smooth,
subimbricate; two precloacal pores; 4/4 femoral pores;
12/11 unpored proximal femoral scales on each side; 7/6
enlarged distal femoral scales. Original tail of holotype
longer than snout-vent length (TAL/SVL ratio 106.9%);
hemipenial bulge greatly swollen (TBW 3.4 mm), homo-
geneous scales on dorsum of the tail directed backwards,
spine-like tubercles along tail; tail with 4—5 enlarged flat-
tened obtuse scales forming whorls; a large, blunt post-
cloacal spur on each side, dorsoventrally flattened and
narrow; a single median series of smooth, irregular, oval
to rhomboid subcaudals.
Forelimbs very short, slender (LAL/SVL ratio 13.3%
and UAL/SVL ratio 13.3%), upper arm and lower arm
equal in size; hind limbs long, tibia slightly shorter
than femur (TBL/SVL ratio 18.0% and FEL/SVL ratio
19.3%). Dorsal, anterior, and posterior surfaces of upper
arm and lower arm with keeled and less imbricate scales
than ventral scales, ventral surfaces with smooth scales,
scales of the anterior surface twice as large as those of the
other aspects. Scales on anterior and posterior surfaces of
femur keeled, dorsal and ventral scales smooth, ventral
scales twice as large as those of the other limb surfaces.
Scales on dorsal, anterior, and posterior surfaces of tibia
keeled, ventral scales smooth, anterior scales twice as
large as those of the other limb surfaces. Manus and pes
with smooth granules dorsally and ventrally; dorsum of
digits with conical granular smooth scales. Digits elon-
gate and slender with inflected distal phalanges, all bear-
ing slightly recurved claws. Subdigital lamellae entire
(except divided at first interphalangial joint), unnotched;
total lamellae on manus (left/right): digit I (10/9), dig-
it It (13/13), digit III (14/13), digit TV (15/14), digit V
(13/14); total lamellae on pes (left/right): digit I (9/9),
digit II (12/13), digit HI (16/15), digit ITV (16/16), digit
V (14/14); interdigital webbing absent; relative length of
left manual digits: I (2.1 mm), V (2.2 mm), II (2.5 mm),
IIT (2.6 mm), IV (3.0 mm); relative length of left pedal
digits: 1 (2.1 mm), II (3.0 mm), III (3.5 mm), V (3.6 mm),
IV (3.8 mm).
Variation of the type series. The SVL of adult speci-
mens in the type series of Cnemaspis kawminiae sp. nov.
(n = 3) ranges from 33.2 to 35.6 mm; interorbital scales
20-22; scales from eye to tympanum 20-22; canthal
scales 10-11; supraciliaries 9-10; tubercles on posterior
flank 7—8; ventral scales 107—114 (Tables 7-8); midbody
scales 76-78, paravertebral granules 86—92, belly scales
across venter 17—21; unpored proximal femorals 11-13
in males, unpored distal femoral scales 6—7 in males; to-
tal lamellae on digit of the manus: digit I (9-10), digit
Amphib. Reptile Conserv.
II (12-13), digit HI (13-14), digit TV (14-15), digit V
(13-14); total lamellae on digit of the pes: digit I (9-10),
digit I (12-13), digit I (15-16), digit IV (15-16), digit
V (14-15).
Color of living specimens. Dorsal body, limb, and tail
generally light grey to brown, with an oblique black line
in the interorbital area, also between eye and nostril; a
wide ‘W’-shaped, black patch on the occipital area with
two median cream-white spots; four scattered, double
“W’-shaped brownish markings on the dorsum of the
trunk with tiny irregular stripes, and ten grey brownish
blotches along the tail (Fig. 10). Lateral side of limbs and
body grey-brown with scattered black spots, and cream
colored lateral conical tubercles on tail and trunk. Three
straight, dark brown postorbital stripes-downwards and
upwards; supraciliaries and nasals greyish brown. Pupil
circular and black with the surrounding scales yellowish
brown, supralabials and infralabials with a median cream
spot. Ventral surfaces of head, body, and limbs beige to
cream, but gular area covered in tiny black spots; ventral
surface of tail cream colored.
Color of preserved specimens. Dorsum cinnamon
brown, with faded double ‘W’-shaped patches on dor-
sum, irregular tiny brown dots on head; faded brown line
between eye and nostrils on both sides, and three brown
postorbital stripes on either side (Fig. 9); venter dirty
white with some scales on throat, abdomen, thigh, tail
base, and arms with dark brown dots.
Etymology. The specific epithet is an eponym Latinized
(kawminiae) in the feminine genitive singular, honoring
Hadunneththi Kawmini Mendis — mother of the first au-
thor (Suranjan Karunarathna) for her unconditional love,
generous support, and financial support for research.
Distribution and natural history. The type local-
ity, Mandaramnuwara (7.020103—7.039953°N and
80.768794—80.807014°E) in the east wet bioclimatic
zone is located at the northern part of Pidurutalagala
mountain range (Fig. 11). This area supports tropical
montane forest vegetation (Gunatilleke and Gunatilleke
1990) with wet evergreen forest. The core study area was
~300 ha in size, at an elevation range ~1,400—1,800 m
asl and annual temperature of 27.4—28.9 °C. Cnemaspis
kawminiae sp. nov. was not abundant in the study area
as only five (+0.1) geckos per surveyor-hour were found
in Mandaramnuwara, This species was found on moss
covered boulders and rock surfaces in forested areas and
well-shaded home gardens with ample woody tree cover
(light intensity: 486-592 Lux); as well as rock walls and
rock crevices along roads. These habitats were very wet
and cool (ambient temperature: 24.2—26.5 °C, substrate
temperature: 26.7—28.3 °C, canopy cover: 70-85% and
relative humidity: 74-92%). The mean annual rainfall of
3,000—4,000 mm is received mainly during the southwest
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Fig. 10. Holotype male of Cnemaspis poe Sp. nov. . (NMSL 2018, 18.01) in life in-situ. (I Dorsal view oi the full body, and
(B) dorsolateral view with labial coloration. Photos: Madhava Botejue.
monsoon (May—September). A total of 26 females, 11
males, and eight juveniles of this species were observed
from twelve sites in the Mandaramnuwara area. Dur-
ing July to September, hatchlings, juveniles, and gravid
females carrying one or two eggs were observed. Eggs
were pure white (mean diameter 5.2 + 0.02 mm), and al-
most completely round in shape with a slightly flattened
side which was often the side attached to the substrate or
between the eggs.
Conservation status. Application of the IUCN Red
List criteria indicates that C. kawminiae sp. nov. 1s
Critically Endangered (CR) due to having an area of
occupancy (AOO) <10 km? (four locations, 0.13 km? in
total assuming a 100 m radius around the georeferenced
location) and an extent of occurrence (EOO) <100 km?
(2.32 km’) in Central Province [Applicable criteria
B2-b (ii1)].
Amphib. Reptile Conserv.
Remarks. Cnemaspis kawminiae sp. nov. most closely
resembles C. kumarasinghei (east intermediate zone)
and C. gotaimbarai (northeast dry zone) morphological-
ly. The type localities of these species are separated by
~80 km (Maragala in Monaragala, ~500 m asl) and ~44
km (Kokagala in Padiyathalawa, ~300 m asl) straight
line distances from Mandaramnuwara (~1,500 m asl) in
Nuwara-Eliya District (Fig. 1). Also see the comparison
with other species for more details.
Discussion
The recent renaissance in the taxonomy and systematics
of genus Cnemaspis has led to a notable increase in spe-
cies richness, particularly from south and south-eastern
Asia, including the Indo-Malayan mainland as well as
Indian-oceanic and south-pacific islands (Iskandar et al.
2017; Riyanto et al. 2017; Wood et al. 2017; Karunara-
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
Fig. 11. General habitats of Cnemaspis
view of the granite hill at roadside, (B) small granite cave close to the stream, and (C) granite rock wall along the road. Photos:
Madhava Botejue.
thna et al. 2019b; Uetz et al. 2019a). With over 160 spe-
cies, Cnemaspis is considered the second-most speciose
gecko genus in the world, after Cyrtodactylus (Grismer
et al. 2014; Present paper). With the inclusion of the three
new species described here, species richness of Cnemas-
pis, the most species-rich reptile genus of Sri Lanka, rises
to 36 (13 species described in year 2019). Similar phy-
logenetic radiations with high degrees of endemism via
complex evolutionary processes have been documented
for snakes, other Gekkonid squamates, and amphib-
ians of Sri Lanka (Bauer et al. 2010; Pyron et al. 2013b;
Meegaskumbura et al. 2019). Our study further bolsters
the notion that Sri Lanka is a hotspot for reptile diver-
sity and endemism (Bossuyt et al. 2004). Since all three
currently described members of this genus are endemic
to the island, Cnemaspis exhibits the greatest degree of
genus-level endemism in Sri Lanka. Sri Lankan Cnemas-
pis species represent two distinct evolutionary lineages,
the kandiana and podihuna clades (Agarwal et al. 2017;
Karunarathna et al. 2019b).
The three new species described in this paper have not
been included in any previous phylogenies of the genus
Amphib. Reptile Conserv.
(Bauer et al. 2007; Agarwal et al. 2017; Karunarathna
et al. 2019b). All of these new species (C. dissanayakai
sp. nov., C. kawminiae sp. nov., and C. kotagamai sp.
nov.) were assigned to the C. kandiana clade based on
the presence of small and irregularly shaped subcaudal
scales (see Karunarathna and Ukuwela 2019). Howev-
er, more in-depth phylogenetic studies are necessary to
confirm the placement of these three new species within
this clade and subgroups (Table 9). Hence, we strongly
recommend broader and more robust molecular phyloge-
netic studies on Cnemaspis species, as well as on other
gecko species, to identify the true richness within the is-
land. Almost all Sri Lankan Cnemaspis species are found
within relatively cool, moist habitats (ambient tempera-
ture: 24.2—32.3 °C; substrate temperature: 25.2—28.7 °C;
relative humidity: 68-92%), with relatively high levels
of canopy cover and high-profile mature trees, and shady
(canopy cover: 60-90%; light intensity: 385-821 Lux)
environments with tall large trees (Karunarathna et al.
2019b). Moreover, all of these new species were found
in granite caves or in association with rocky substrates.
Such aspects of natural history and microhabitat selec-
December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
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December 2019 | Volume 13 | Number 2 | e216
345
Amphib. Reptile Conserv.
Three new species of Cnemaspis from Sri Lanka
tion of these new species are com-
parable to other congeners, which
imply niche conservatism among
divergent lineages.
The bulk of these rupicolous
geckos are restricted to cool,
moist, shady granite caves and
rock walls or under granite boul-
ders. According to our findings
these geckos prefer narrow (~3—4
mm), long (~100-400 mm), and
deep (~20—180 mm) crevices as
refugia and oviposition sites. In
several surveyed locations with
granite caves, we were unable to
find Cnemaspis species due to the
lack of tall shady trees and ad-
equately cool temperatures (sub-
strate temperature: 25.2—28.7°C).
A majority (66.7%) of Cnemaspis
Species are restricted to the wet
bioclimatic zones of Sri Lanka
and are point-endemic microhabi-
tat specialists where distribution
ranges are limited to <100 km”.
The restricted distribution could
be an artifact of the limited avail-
ability of caves and similar mi-
croenvironments with granite or
rock-based substrates. The high
species richness in Sri Lanka may
be accounted by the possibility
of multiple, independent coloni-
zation events from the Indian
mainland with subsequent, geo-
graphically-isolated in-situ spe-
ciation. The majority of the Indian
Cnemaspis species have not been
comparatively analyzed alongside
the Sri Lankan species (Agarwal
et al. 2017; Karunarathna et al.
2019b). The three new species
described here are recorded from
isolated locations in wet, interme-
diate, and dry bioclimatic zones of
Sri Lanka. Of these, C. kawminiae
sp. nov. is described from the wet
zone montane region; C. kotaga-
mai sp. nov. 1s described from the
intermediate zone lowland; and C.
dissanayakai sp. nov. is described
from the dry zone lowland (Table
10). The record of C. kawminiae
sp. nov. from Mandaramnuwara
is noteworthy, as this is a high-
altitude location nestled in the
central highlands (1,400—1,800 m
2
<
Y
&
Ss
i)
a)
|
—_~
=
~
=
—}
i)
te
o)
Group (2) — podihuna
ss oo | se [se [se [one] ve [oe forlorn] + Poe [ef mm f 9
soo [ [se [oy [ons] oe [re [oem] = [ore foes] = Pos [oo [om | os
se for] se [se [oy [one] sn] v9 [war [ sa] ve fem [al es | — [orem | 2m
C. nandim-
C. anslemi
C. hitihami
C. kohukum-
C. nilgala
C. phillipsi
C. punctata
C. rajakarunai
C. rammalen-
C. molligodai
C. podihuna
SUP — Supralabials, INF — Infralabials, PG — Paravertebral granules, IFS — Interfemoral scales, FLSP — Flank spines, PCP — Precloacal pores, FP — Femoral pores, HET — Heterogeneous, HOM
C. gemunu
— Homogeneous, KD — Keeled, SM — Smooth.
Table 9 (continued). Key characters of 36 currently known Cnemaspis species in Sri Lanka. Abbreviations: mm — Millimeters, SVL — Maximum Snout to vent length, SUB — Subcaudals,
Amphib. Reptile Conserv. 346 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
i ‘ £ i
Fe. ' F
1 Poe ah be T
5 1 Bot etal Nag ei aes
; ‘ ra = a - 3 = f
L -. . faire A fae f :
s ‘ ; . as * Sept |
a Ls, re, Ea - : st af
ey
ies it ah. 4} 4 ae.
AE SSS ke
Fig. 12. Threats to the isolated hill forests and Cnemaspis species in study areas in Sri Lanka. (A) Illegal forest clearing, (B) fire-
wood collection for tea factory, (C) granite mining activities, (D) agricultural fields in slopy areas, (E) tea plantation and highly
crowded anthropogenic habitat, and (F) a landslide in mountain areas. Photos: Suranjan Karunarathna and Madhava Botejue.
asl), making this the 4" species in the genus found at an
elevation above 1,000 m asl.
Bambaragala and Dimbulagala are isolated residual
mountains and rock outcrops embedded within a forest
and features granite caves incorporated with historical
Buddhist monasteries, whereas Mandaramnuwara is a
mixture of forested areas and rural human habitation. All
these habitats are susceptible to human-induced habitat
degradation, including clear cutting and timber felling,
forest fragmentation, granite mining, tea cultivation (Fig.
12), rubber cultivation, vegetable farming, invasive spe-
cies, human settlements, road and other infrastructure
development, and waste disposal (see Karunarathna et
Amphib. Reptile Conserv.
al. 2017). Bambaragala, situated in Ratnapura District of
Sabaragamuwa Province, is the most vulnerable habitat
as it is a small forested rock outcrop (~50 ha) located
amidst a rapidly urbanizing landscape; where a part of
the rock outcrop is currently undergoing mining, mak-
ing C. kotagamai sp. nov. the most endangered amongst
these new species. However, many such habitats are
somewhat protected due to the presence of Buddhist
monasteries which serve as refugia for reptiles and oth-
er faunal groups, and it is imperative to conserve these
habitats to protect the island’s unique biodiversity (Ama-
rasinghe et al. 2016; Edirisinghe et al. 2018; Karunara-
thna et al. 2019a). Sri Lanka’s tropical humid wet zone is
December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
globally recognized for its exceptionally high biodiver-
sity and endemism (Bossuyt et al. 2004). Nonetheless,
the new species reported here and in previous studies on
the same genus continue to illustrate the undocumented
diversity of Cnemaspis that also occurs within the dry
and intermediate bioclimatic zones (Batuwita et al. 2019;
Karunarathna et al. 2019b).
Most of the Cnemaspis species from the dry and in-
termediate climatic zones of Sri Lanka are, however, re-
stricted to small isolated habitats scattered over the low-
lands (Batuwita et al. 2019; Karunarathna et al. 2019a,b).
The presence of granitic caves and the humid forest cover
surrounding the caves seem to serve as ideal refugia for
these geckos with narrow, specialized ecological niches.
It is very likely that future studies on the biogeography of
Cnemaspis in Sri Lanka will highlight the importance of
these isolated habitats in generating and maintaining the
diversity of these unique groups of geckos in the island
(Karunarathna and Amarasinghe 2011; Amarasinghe et
al. 2016). At the same time, it is important to note that the
point endemic species described here, which are highly
sensitive to changes in the habitat, would be severely af-
fected by habitat degradation. Hence, past and present
studies have emphasized the importance of conserving
such isolated habitats throughout the country (Karunara-
thna and Amarasinghe 2013; Gabadage et al. 2018).
Though traditional conservation strategies usually target
extensive natural habitats to maximize biodiversity con-
servation, our studies indicate that these small isolated
habitats also deserve the immediate attention of conser-
vation authorities. Thus, we believe our findings on these
geckos and their granite cave and rock-associated habi-
tats add a new dimension to the biodiversity conservation
of Sri Lanka.
fo
CR
Relative
humidity
Light
intensity
(Lux)
469
385
448
455
648
594
617
625
592
566
486
578
Substrate
temperature
29.8 °C 28.1 °C
Ambient
temperature
30.6 °C 28.6 °C
29.6 °C 27.8 °C
24.2 °C 28.3 °C
temperature
1,500- “
2,000 27.8-29.6 °C
: 28.9-30.2 °C
3,000- i
4,000 27.4—28.9 °C
Rainfall
(mm)
500-
000
1
2
Microhabitat
Granite cave
Granite cave
Old building
Granite cave
Granite cave
Old building
Old building
Granite wall
Granite wall
Granite wall
Semiever-
evergreen
Wet
evergreen
Acknowledgements.—We thank Chandana Sooriyabandara
(Director General of Department of Wildlife Conserva-
tion), Laxman Peiris (Research Director of Department
of Wildlife Conservation), the research committee, the
field staff of the Department of Wildlife Conservation
(WL/3/2/1/14/12, and WL/3/2/42/18a,b), and the Conser-
vator General of Forests and the staff of Forest Department
(FRC/5, and FRC/6) for granting permission and provid-
ing help during the field surveys; and Nanda Wickramas-
inghe, Sanuja Kasthuriarachchi, Chandrika Munasinghe,
Rasika Dasanayake, Ravindra Wickramanayake, and P.
Gunasiri at NMSL for assisting while examining collec-
tions under their care. Ashan Geeganage (for Fig. 8b), Hat-
angala Medhananda thero, Buddika Madurapperuma (for
the GIS map), Chamara Amarasinghe, Tharaka Kusum-
inda, Hasantha Wijethunga, D.M. Karunarathna, Kawmini
Karunarathna, Rashmini Karunarathna, and Thesanya Ka-
runarathna provided valuable assistance. This work was
mainly supported by Nagao Natural Environment Foun-
dation (2018-20) grant to SK, and United States National
Science Foundation grants DEB 1555968 and EF 1241885
(subaward 13-0632) to AMB. Finally, we would like to
139m
1,600 m
1,592 m
7.020600 80.788639 1,658 m
7.034775 80.783497 1,574 m
Bo
ge
ec
Ss
§ 2 = fn
= 3 oS S
< A =
=
2
-—
S
>
ic)
—
‘ae Ee
ANTENITn
aio
OIiNT
SIOATN
nap ora
OTN] co
WmM_WO TT
m~P_Re]e
o;Toy]o
coyTo} co
colraotwo
Ge | oO} co
NIENITOR
NANT mI] oO
as To ITLN
WTO TE”
‘Oo | © | ©
80.746783
81.135569
81.141675
81.114836
81.127831
80.798794
80.773903
Coordinates
Le fe |
6.510536
7.872931
7.851358
7.860200
7.850547
7.033558
7.028314
District
Ratna-
pura
Polon-
Se
Wet zone
Nuwara-
Bioclimatic
Intermedi-
ate zone
C. kotagamai
dissanayakai
C. kawminiae
C.
Table 10. Distribution and ecological data of the three new Cnemaspis species from Sri Lanka. Abbreviations: m — meters; ha — hectares; mm — millimeters; Lux — light intensity; CR — Criti-
cally Endangered.
Amphib. Reptile Conserv. 348 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
thank Kelum Manamendra-Arachchi, Thasun Amarasing-
he, Craig Hassapakis and Michael Grieneisen for various
support, and anonymous reviewers for their constructive
criticism of an earlier draft that helped to significantly im-
prove this paper.
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Suranjan Karunarathna began his scientific exploration of biodiversity with the Young Zoologists’
Association of Sri Lanka (YZA) in early 2000, and led the society in 2007 as the President. Suranjan
earned his Masters of Environmental Management from University of Colombo, Sri Lanka, in 2017.
As a wildlife researcher, he studies herpetofaunal ecology and taxonomy, and also promotes science-
based conservation awareness on the importance of biodiversity and its conservation among the Sri
Lankan community. Suranjan is an active member of several specialist groups of IUCN/SSC, and
has served as an expert committee member of the IUCN Global and National Red List development
December 2019 | Volume 13 | Number 2 | e216
Amphib. Reptile Conserv.
Karunarathna et al.
Anslem de Silva M.Sc., D.Sc. (University of Peradeniya, Sri Lanka) started keeping reptiles
at the early age of seven, and he has taught herpetology at the Rajarata University of Sri Lanka
and mentored final-year veterinary students at University of Peradeniya. Anselm has conducted
herpetofaunal surveys in most of the important ecosystems in the country, and has published more
than 400 papers, of which nearly 60 are books or book chapters. Anslem had done yeoman service
to the country and the region for more than 50 years. He is the Regional Chairman of the Crocodile
Specialist Group for South Asia and Iran, Co-Chair of the Amphibian Specialist Group IUCN/SSC
Sri Lanka. Anslem received the IUCN/SSC Sir Peter Scott Award for Conservation Merit in October
2019 — the first Sri Lankan to receive this prestigious award.
Madhava Botejue has been engaged in research on the biodiversity, ecology, distribution,
behavior, taxonomy, and conservation of Sri Lankan fauna for the past 14 years, with a main focus
on herpetofauna, avifauna, and mammals. Madhava has contributed to environmental protection
through many community-based awareness programs on the importance of biodiversity and its
conservation. He earned his B.Sc. degree in Natural Sciences from The Open University of Sri
Lanka in 2009. Currently, he serves as an Environmental Officer at the Central Environmental
Authority, Sri Lanka, a member of IUCN/SSC Crocodile Specialist Group, and an expert committee
member of IUCN Global and National Red List development programs.
Dinesh Gabadage is a field biologist who began his wildlife interests in 1990 as a member of the
Young Zoologists Association of Sri Lanka (YZA), and also in 1994 as a member of the Wildlife
Heritage Trust of Sri Lanka (WHT). Dinesh is a dedicated researcher studying the biodiversity
ecology, distribution, behavior, and taxonomy of herpetofauna, avifauna, and mammals in Sri
Lanka; and he has conducted many community-based programs promoting wildlife conservation.
He is also an expert committee member in the IUCN Global and National Red List development
programs, and earned his Diplomas in Palaeo-biodiversity and Zooarchaeology from University of
Kelaniya, Sri Lanka.
Lankani Somaratne, B.Sc. (University of Colombo, Sri Lanka), is a zoologist who started her
career as an Assistant Director in the Zoology Division of the Department of National Museums five
years ago. Lankani has engaged in re-cataloging and updating of the avifaunal, skink, amphibian,
and ichthyological collections at the National Museum for the past five years. She has contributed to
enhancing the knowledge on the museological aspects of Natural Specimen conservation for different
communities. She is a member of the International Community of Museums (ICOM), representing
Sri Lanka. Apart from zoological conservation, she is currently working on conservation project at
the Dutch Museum, Sri Lanka.
Angelo Hettige began his interest in wildlife from a very young age. His interests began to grow
as a member of the Young Zoologists Association of Sri Lanka (YZA) since the early 2000s, from
the junior group continuing up to the senior group. Angelo has contributed to conservation through
community awareness programs on the importance of reptiles and their conservation, and through
numerous snake rescues. Currently, he is working in the snake anti-venom research project at the
University of Peradeniya, Sri Lanka, and he wishes to continue his career studying herpetofauna
and its conservation.
Nimantha Aberathna is a naturalist who began his career and wildlife interests in 2004 as a
naturalist, and as a member of the Youth Exploration Society of Sri Lanka (YES) in 2009. He served
as the President of the Research and Education Committee during 2015-2017. Nimantha holds a
certificate of Wildlife Conservation and Management from the Open University of Sri Lanka. As
a wildlife researcher, he is studying ichthyofauna and orchid ecology and taxonomy. He is also
engaged in a captive breeding program for threatened species, and has been involved in many snake
rescue events. Nimantha worked as a venom extractor for the snake anti-venom research project at
the University of Peradeniya, Sri Lanka.
Majintha Madawala is a naturalist who began his career and wildlife interests in 1995 as a member
of the Young Zoologists Association of Sri Lanka (YZA), and holds a Diploma in Biodiversity
Management and Conservation from the University of Colombo, Sri Lanka. As a conservationist
and a naturalist, he is engaged in numerous habitat restoration, snake rescue programs, and
biodiversity research projects in Sri Lanka. Currently, Majintha is engaged in herpetofaunal research
with the Victorian Herpetological Society in Australia. He is also an active member of the IUCN/
SSC Crocodile Specialist Group and IUCN Global and National Red List development programs.
351 December 2019 | Volume 13 | Number 2 | e216
Amphib. Reptile Conserv.
Three new species of Cnemaspis from Sri Lanka
Gayan Edirisinghe began his studies on wildlife in 2000 when he became a member of the
Young Zoologists Association of Sri Lanka (YZA), which laid a strong foundation for his interest
in mammals. Gayan initiated his research career in 2005 with a study on small mammals. For
the past ten years, he has been involved in many research projects on Sri Lankan fauna, mainly
focusing on the diversity, distribution, ecology, behavior, and conservation of chiropterans. He has
conducted awareness programs to educate the community on the importance of biodiversity and its
conservation, and earned his Diplomas in Palaeo-biodiversity and Zoo-archaeology from University
of Kelaniya, Sri Lanka.
Nirmala Perera has been a member of Young Zoologists’ Association (YZA) since 1999, and he
has conducted several awareness programs on biodiversity conservation through many different
levels of the society. Nirmala also served as the secretary of the action committee of YZA, and
he has worked actively on several environmental issues raised in Sri Lanka. He holds a Diploma
in Biodiversity Management from the University of Colombo and worked as the snake biologist
in the snake venom research project in the Faculty of Medicine, University of Colombo. He also
worked as a Project Coordinator at Udawalawe Human-Elephant Conflict Program of the Born Free
Foundation, Sri Lanka (2011-2014).
Sulakshana Wickramaarachchi is a hardware and software engineer by profession, but began his
studies on wildlife conservation in 2006 as a member of the Young Zoologists’ Association (YZA),
and later served as a committee member of the Research Committee and as the Treasurer during
2011-2012. He is also engaged in captive breeding programs for threatened species and many
snakes rescue missions. He also conducts awareness programs to promote the importance of snake
fauna and its conservation among the Sri Lankan community. Also he worked as an assistant venom
extractor of the snake venom research project in the Faculty of Medicine, University of Colombo.
Thilina Surasinghe is an Assistant Professor in the Department of Biological Sciences in
Bridgewater State University, Mssachusetts, USA, and obtained his Ph.D. in Wildlife Biology
at Clemson University, South Carolina, USA. Thilina is an ecologist; his academic training
encompasses different aspects of biology, ecology, environmental sciences, and natural resources
management. He is experienced in teaching undergraduates in biology, environmental sciences, and
social sciences; and he takes part in projects on landscape-scale biodiversity assessments, Red List
assessments, conservation planning, GIS based threat and GAP analyses, and EPA protocols.
Niranjan Karunarathna is a naturalist who loves traveling, camping, and hiking. He has been a
member of Young Zoologists’ Association (YZA) since 2006, has participated in many herpetological
research projects and also has ongoing funded projects. Niranjan is also conducting wildlife
photography, biodiversity conservation, and educational programs for the Sri Lankan community.
Mendis Wickramasinghe founded the Herpetological Foundation of Sri Lanka (HFS), to further
pursue independent research on the herpetofauna of Sri Lanka, while providing a platform for young
herpetologists to initiate research. With nearly 25 years of field research experience on the herpetofauna
of Sri Lanka, his work has focused on taxonomic identification and biodiversity assessments of
amphibians and reptiles, in an effort to increase awareness on the importance of conserving their
habitats in Sri Lanka. As a result, he has been able to discover and describe 29 new species of
amphibians and reptiles, and participated in the re-discovery of three “extinct” amphibian species.
Kanishka D.B. Ukuwela is currently a Senior Lecturer in Zoology at the Rajarata University of Sri
Lanka. He holds a B.Sc. (Hons.) degree in Zoology from the University of Peradeniya, Sri Lanka
and a Ph.D. in Evolutionary Biology from the University of Adelaide, Australia. His current research
focuses on the origins, evolution, systematics, and conservation of the South Asian herpetofauna.
Aaron Bauer grew up collecting reptiles and amphibians in his native New York. He is the Gerald M.
Lemole Endowed Professor of Integrative Biology at Villanova University in Pennsylvania, USA,
and has been studying reptiles, especially geckos, for more than 35 years. Aaron has worked widely
in Sri Lanka, India, southern Africa, Australia, and the South Pacific; and has described nearly 200
species of reptiles and written more than 750 publications. He is a former Secretary General of the
World Congress of Herpetology, President of the Society for the Study of Amphibians and Reptiles,
President of the Herpetologists’ League, and Chairman of the Herpetological Association of Africa.
352 December 2019 | Volume 13 | Number 2 | e216
Karunarathna et al.
Appendix 1.
Comparative Cnemaspis materials examined from Sri Lanka
Cnemaspis alwisi: NMSL 2004.09.01 (holotype), NMSL 2004.09.02 (paratype), NMSL 2004.09.03 (paratype), WHT 5918, WHT
6518, WHT 6519, WHT 7336, WHT 7337, WHT 7338, WHT 7343, WHT 7344, WHT 7345, WHT 7346.
C. anslemi: NMSL 2019.14.01 (holotype), NMSL 2019.14.02 (paratype), NMSL 2019.14.03 (paratype).
C. amith. BMNH 63.3.19.1066A (holotype), BMNH 63.3.19.1066B (paratype), BMNH 63.3.19.1066C (paratype).
C. butewai: NMSL 2019.07.01 (holotype), NMSL 2019.07.02 (paratype), NMSL 2019.07.03 (paratype).
C. gemunu: AMB 7495 (holotype), AMB 7507 (paratype?), WHT 7221, WHT 7347, WHT 7348, NMSL 2006.11.01, NMSL
2006.11.02, NMSL 2006.11.03, NMSL 2006.11.04.
C. godagedarai: NMSL 2019.09.01 (holotype), NMSL 2019.16.01 (paratype), NMSL 2019.16.02 (paratype).
C. gotaimbarai: NMSL 2019.04.01 (holotype), NMSL 2019.04.02 (paratype), NMSL 2019.04.03 (paratype).
C. hitihami: NMSL 2019.06.01 (holotype), NMSL 2019.06.02 (paratype), NMSL 2019.06.03 (paratype).
C. ingerorum: WHT 7332 (holotype), WHT 7330 (paratype), WHT 7331 (paratype).
C. kallima: WHT 7245 (holotype), WHT 7222 (paratype), WHT 7227 (paratype), WHT 7228 (paratype), WHT 7229 (paratype),
WHT 7230 (paratype), WHT 7239 (paratype), WHT 7249 (paratype), WHT 7251 (paratype), WHT 7252 (paratype), WHT 7253
(paratype), WHT 7254 (paratype), WHT 7255 (paratype).
C. kandambyi: WHT 9466 (holotype), WHT 9467 (paratype).
C. kandiana. BMNH 53.4.1.1 (lectotype), BMNH 80.2.2.119A (paralectotype), BMNH 80.2.2.119B (paralectotype), BMNH
80.2.2.119C (paralectotype), WHT 7212, WHT 7213, WHT 7267, WHT 7305, WHT 7307, WHT 7308, WHT 7310, WHT 7313,
WHT 7319, WHT 7322.
C. kivulegedarai: NMSL 2019.08.01 (holotype), NMSL 2019.08.02 (paratype), NMSL 2019.08.03 (paratype).
C. kohukumburai: NMSL 2019.05.01 (holotype), NMSL 2019.05.02 (paratype), NMSL 2019.05.03 (paratype).
C. kumarasinghei: NMSL 2006.13.01 (holotype), NMSL 2006.13.02 (paratype).
C. latha: WHT 7214 (holotype).
C. menikay: WHT 7219 (holotype), WHT 7218 (paratype), WHT 7349 (paratype).
C. molligodai: NMSL 2006.14.01 (holotype), NMSL 2006.14.02 (paratype), NMSL 2006.14.03 (paratype), NMSL 2006.14.04
(paratype), NMSL 2006.14.05 (paratype).
C. nandimithrai: NMSL 2019.01.01 (holotype), NMSL 2019.01.02 (paratype), NMSL 2019.01.03 (paratype).
C. nilgala: NMSL 2018.07.01 (holotype), NMSL 2018.06.01 (paratype), NMSL 2018.06.02 (paratype), NMSL 2018.06.03 (para-
type).
C. pava. WHT 7286 (holotype), WHT 7281 (paratype), WHT 7282 (paratype), WHT 7283 (paratype), WHT 7285 (paratype), WHT
7288 (paratype), WHT 7289 (paratype), WHT 7290 (paratype), WHT 7291 (paratype), WHT 7292 (paratype), WHT 7293 (para-
type), WHT 7294 (paratype), WHT 7295 (paratype), WHT 7296 (paratype), WHT 7297 (paratype), WHT 7298 (paratype), WHT
7299 (paratype), WHT 7300 (paratype), WHT 7301 (paratype), WHT 7302 (paratype).
Amphib. Reptile Conserv. 353 December 2019 | Volume 13 | Number 2 | e216
Three new species of Cnemaspis from Sri Lanka
C. phillipsi. WHT 7248 (holotype), WHT 7236 (paratype), WHT 7237 (paratype), WHT 7238 (paratype).
C. podihuna: BMNH 1946.8.1.20 (holotype), NMSL 2006.10.02, NMSL 2006.10.03, NMSL 2006.10.04.
C. pulchra. WHT 7023 (holotype), WHT 1573a (paratype), WHT 7011 (paratype), WHT 7021 (paratype), WHT 7022 (paratype).
C. punctata: WHT 7256 (holotype), WHT 7223 (paratype), WHT 7226 (paratype), WHT 7243 (paratype), WHT 7244 (paratype).
C. rajakarunai: NMSL 2016.07.01 (holotype), DWC 2016.05.01 (paratype), DWC 2016.05.02 (paratype).
C. rammalensis: NMSL 2013.25.01 (holotype), DWC 2013.05.001.
C. retigalensis: NMSL 2006.12.01 (holotype), NMSL 2006.12.02 (paratype), NMSL 2006.12.03 (paratype), NMSL 2006.12.04
(paratype).
C. samanalensis: NMSL 2006.15.01 (holotype), NMSL 2006.15.02 (paratype), NMSL 2006.15.03 (paratype), NMSL 2006.15.04
(paratype), NMSL 2006.15.05 (paratype).
C. scalpensis: NMSL 2004.01.01 (neotype), NMSL 2004.02.01, NMSL 2004.03.01, NMSL 2004.04.01, WHT 7265, WHT 7268,
WHT 7269, WHT 7274, WHT 7275, WHT 7276, WHT 7320.
C. silvula: WHT 7208 (holotype), WHT 7206 (paratype), WHT 7207 (paratype), WHT 7209 (paratype), WHT 7210 (paratype),
WHT 7216 (paratype), WHT 7217 (paratype), WHT 7018, WHT 7027, WHT 7202, WHT 7203, WHT 7220, WHT 7354, WHT
7333.
C. tropidogater: BMNH 71.12.14.49 (lectotype), NMSL 5152, NMSL 5151, NMSL 5159, NMSL 5157, NMSL 5970, NMSL 5974.
C. upendrai: WHT 7189 (holotype), WHT 7184 (paratype), WHT 7187 (paratype), WHT 7188 (paratype), WHT 7181 (paratype),
WHT 7182 (paratype), WHT 7183 (paratype), WHT 7185 (paratype), WHT 7190 (paratype), WHT 7191 (paratype), WHT 7192
(paratype), WHT 7193 (paratype), WHT 7194 (paratype), WHT 7195 (paratype), WHT 7196 (paratype), WHT 7197 (paratype),
WHT 7260 (paratype).
Amphib. Reptile Conserv. 354 December 2019 | Volume 13 | Number 2 | e216
Official journal website:
amphibian-reptile-conservation.org
Editorial
Amphibian & Reptile Conservation
13(2): xxx—xxxi (€217).
Manuscript reviewers for Amphibian & Reptile Conservation (2019)
Citation: Hassapakis CL, Grieneisen ML, Conradie W. 2019. Manuscript reviewers for Amphibian & Reptile Conservation (2019). Amphibian & Reptile
Conservation 13(2): xxx—xxxi (e217).
Copyright: © 2019 Hassapakis et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribu-
tion 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 30 December 2019; Accepted: 30 December 2019; Published: 31 December 2019
In 2019, ARC published 49 numbered items, including
45 peer-reviewed articles, 3 book reviews, and a collec-
tion of personal tributes to the late Bill Branch. We are
very grateful to the peer-reviewers listed below for vol-
unteering their time and expertise to help us determine
which of the submitted manuscripts that passed our ini-
tial screening merited publication, and also for providing
suggestions that improved the analysis, interpretation,
and presentation of the data and ideas in each article. The
following individuals have provided either manuscript
reviews during 2019 or prior reviews of manuscripts
that were published in 2019 (Volume 13). The names of
those who reviewed more than one manuscript are given
in bold. We look forward to the continuing generous gift
of time from the reviewers who will help us maintain the
high quality of articles published in ARC in the future.
The primary affiliations of these reviewers include
40 countries: Argentina, Bangladesh, Brazil, Bulgaria,
Canada, China, Colombia, Costa Rica, Czech Republic,
Ecuador, England, Germany, Greece, Guatemala, Hon-
duras, India, Indonesia, Israel, Italy, Japan, Malaysia,
Mexico, Netherlands, New Zealand, Pakistan, Panama,
Peru, Portugal, Romania, Russia, Scotland, Serbia, South
Africa, Spain, Switzerland, Turkey, Ukraine, USA, Ven-
ezuela, and Vietnam.
Stephenson Hallison Formiga Abrantes (Brazil)
Alberto Abreu Grobois (Mexico)
Manuel E. Acevedo (Guatemala)
Bahadir Akman (Turkey)
Muhammed Muassir Ali (Turkey)
Matthew C. Allender (USA)
Ronn Altig (USA)
Steven Anderson (USA)
Manuel Aranda (Mexico)
Adrian Armstrong (South Africa)
Alejandro Arteaga (Ecuador)
César Luis Barrio Amordos (Costa Rica)
Jude Brooke (USA)
Luis Daniel Avila Cabadilla (Mexico)
Ernst Baard (South Africa)
James Barnett (Canada)
ee pte Zee ee
Sa SS
Gy Ga Nor
16.
Correspondence. arc.publisher@gmail.com
Amphib. Reptile Conserv.
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34.
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37.
38.
39.
. Jelka Crnobrnyja-Isailovic (Serbia)
. Fabio German Cupul Magafia (Mexico)
. Indraneil Das (Malaysia)
. Carlos Delgado-Trejo (Mexico)
. Jesse Delia (USA)
. Leida Dos Santos (New Zealand)
. Lourdes Echevarria (Peru)
. Eduardo G. Etchepare (Argentina)
. Vanda Lucia Ferreira (Brazil)
. Frederico Gustavo R. Franga (Brazil)
. S.R. Ganesh (India)
. Ana Bertha Gatica Colima (Mexico)
. Victor Hugo Gonzalez Sanchez (Mexico)
. Irene Goyenechea (Mexico)
. Eva Gracia (Spain)
. Monica Guerra (Ecuador)
. Amanda Guthrie (USA)
. Vicente Guzman Hernandez (Mexico)
. Md. Kamrul Hasan (Bangladesh)
Abel Antonio Batista Rodriguez (Panama)
Aaron Bauer (USA)
Chris Beirne (USA)
David Blackburn (USA)
Sergé Bogaerts (Netherlands)
Wolfgang Bohme (Germany)
Leo J. Borkin (Russia)
Donald Brown (USA)
Marius Burger (South Africa)
Patricia A. Burrowes (USA)
Henrique Caldeira Costa (Brazil)
Jonathan Campbell (USA)
Carlos Eduardo Costa de Campos (Brazil)
Onur Candan (Turkey)
Fernando Castro Herrera (Colombia)
Luis Ceriaco (Portugal)
Gerardo Chaves (Costa Rica)
Marcio Chaves (Brazil)
Wei Chen (China)
Basundhara Chettri (India)
Kerim Cicek (Turkey)
Ibrahim Hakki Cigerci (Turkey)
Andrea Costa (Italy)
December 2019 | Volume 13 | Number 2 | e217
ake
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61.
62.
63.
64.
65,
66.
67.
68.
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Md. Mosharrof Hossain (Bangladesh)
Michael Itgen (USA)
Ulrich Joger (Germany)
Gregor Jongsma (USA)
Mert Karis (Turkey)
M. Monirul H. Khan (Bangladesh)
Akin Kirag (Turkey)
David Kizirian (USA)
Panagiotis Kornilios (Spain)
Brian Kubicki (Costa Rica)
Mirza Kusrini (Indonesia)
Elizabeth Labastida Estrada (Mexico)
James Labisco (England)
William W. Lamar (USA)
Sebastian Lotzkat (Germany)
Vinh Quang Luu (Vietnam)
Fabio Maffei (Brazil)
Stephen Mahony (England)
Anita Malhotra (England)
Ricardo Luria Manzano (Mexico)
Vicente Mata-Silva (USA)
Jose Antonio Mateo Miras (Spain)
Daniel Medina (Brazil)
Shai Meiri (Israel)
+Joseph Mitchell (USA)
Ivelin Mollov (Bulgaria)
Irina T. Morales Castafio (Colombia)
John Mulder (Netherlands)
Edgar E. Neri-Castro (Mexico)
Noorun Nisa (Pakistan)
Cristiano Campos Nogueira (Brazil)
Kei Okamoto (Japan)
Dario Ottonello (Italy)
Andrés Leonardo Ovalle (Colombia)
Cansu Ozbayer (Turkey)
Panayiotis Pafilis (Greece)
Davi Lima Pantoja Leite (Brazil)
Theodore J. Papenfuss (USA)
Gabriela Parra-Olea (Mexico)
Johannes Penner (Germany)
Darren Pietersen (South Africa)
100. Daniel Pincheira-Donoso (England)
101.Juan M Pleguezuelos (Spain)
102. Louis Porras (USA)
Craig Hassapakis, Founder, Publisher, Co-editor
Michael L. Grieneisen, Co-editor
Werner Conradie, Africa Regional Editor
Amphib. Reptile Conserv.
Hassapakis et al.
103.Cynthia P.A. Prado (Brazil)
104. Alex Pyron (USA)
105.Gustavo Ernesto Quintero Diaz (Mexico)
106.Aurelio Ramirez-Bautista (Mexico)
107. Kelsey Reider (USA)
108.Roberto Luna Reyes (Mexico)
109. Mark-Oliver R6del (Germany)
110. Liliana Patricia Saboya Acosta (Colombia)
111. Xavier Santos Santiro (Portugal)
112. Ulrich Schepp (Germany)
113.Gustavo J. Scrocchi (Argentina)
114.Celsi Sefiaris (Venezuela)
115. Shirley Jennifer Serrano Rojas (Scotland)
116. Neftali Sillero (Portugal)
117.Roberto Sindaco (Italy)
118. Ulrich Sinsch (Germany)
119. Brian Slough (Canada)
120. Jiti Smid (Czech Republic)
121.Alexandru Strugariu (Romania)
122. Bryan Stuart (USA)
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132.Gernot Vogel (Germany)
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137.Steven Whitfield (USA)
138. Larry David Wilson (Honduras)
139.Deniz Yalcinkaya (Turkey)
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141.Tonglei Yu (China)
142. Robert T. Zappalorti (USA)
143.Bao Zhang (China)
144.Guangzhou Zhou (China)
145.Oleksandr Zinenko (Ukraine)
146.Marco Alberto Luca Zuffi (Italy)
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